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Its Domestication and Behavior 

other books by the author: 

Canine Behavior 
Canine Pediatrics 

Integrative Development of Brain and Behavior in the Dog 
The Behavior of Wolves, Dogs and Related Canids 
Understanding Your Cat 
Understa?:ding Your Dog 

Concepts in Ethology: Animal and Human Behavior 
Betiveai Animal and Man, The Key to the Kingdom 
The Wild Canids: Their Systematics, Behavioral Ecology and 



Its Domestication and Behavior 

Michael W. Fox 

Director, Institute for the Study of Animal Problems 
Humane Society of the United States, Washington, D.C. 

Garland STPM Press 

Nezu York & London 

Copyright © 1978 by Michael W. Fox 

All rights reserved. No part of this work covered by the copyright hereon may be 
reproduced or used in any form or by any means — graphic, electronic, or 
mechanical, including photocopying, recording, taping, or information storage 
and retrieval systems — without permission of the publisher. 

15 14 13 12 11 10 9 8 7 6 5 4 3 2 1 

Library of Congress Cataloging in Publication Data 

Fox, Michael W 1937- 
The dog. 

Bibliography: p. 

Includes index. 

1. Dogs— -Behavior. 2. Canldae— Behavior. 

3. Domestication. 4. Mammals— Behavior, J, TiiJe- 
SF433.F69 599'.74442'045 76-57852 

ISBN 0-8240-9858-7 

CarUnd STTM Press. 

A division of Garland Publishing, Inc. 


Acknowledgments vii 

Introduction i 

I. Effects of Domestication in Animals: A Review 3 

II. Sodo-Ecology of Wild Canids: Environment 

and Behavioral Adaptation 21 

III. Behavior and Ecology of an Urban Feral Dog 

Pack 41 

IV. Vocalizations in Wild Canids and Possible 

Effects of Domestication 69 

V. Behavior Genetics of F, and F; CoyotexDog 

Hybrids 9 ' 

VI. Effects of Domestication on Prey-Catching 
and Killing in Domesticand Wild Canids and 

F:; Hybrids m- 


VII. Interspedes Interaction Differences in Play 

Actions in Canids 133 

Vin. Sodalization Patterns in Hand-Reared Wild 

and Domesticated Canids 141 

DC. Stages and Periods in Development: 

Environmental Influences and Domestication 153 

X. Behavior, Development, and 

Psychopathology of Cardiac Activity in the 

Dog 177 

XL Condusions: Domestication and Man-Dog 

Relationships 235 

Appendix I 263 

Appendix 11 267 

Appendix III 271 





The author gratefully acknowledges the collaboration of the follow- 
ing undergraduate assistants and colleagues in the completion of 
some of the material included in this book: Keith Kretchmer (Chap- 
ter I), Ellen Blackman and Dr. Alan Beck (Chapter 3), and James 
Cohen (Chapter 4). I am espedally glad for the opportunity to 
include some of my Army research data collected in collaboration 
with Dr. Jeff Linn (Chapter 10) and to reevaluate this material from 
the original report (Linn, 1974) in relation to other data derived 
from wild canids and their hybrids in my laboratory. Thanks also to 
Dr. R. V. Andrews for making the plasma cortisol estimations in 
the wolf cubs which are included in this report. 

Much of the material incorporated in this text, some of which 
has been published separately as short artides in sdentific jour- 
nals, constitutes an integrated series of studies which provides a 
valuable multidimensional view of domestication and behavior. 

My research was supported in part by NSF grant GB-34172, 
PHS grant P 10-ES-00139 awarded through the Center for the Biol- 
ogy of Natural Systems, Washington University, and a grant from 
the Arctic Institute of North America under contractual arrange- 
ment with the Office of Naval Research. 

Thanks also to Ms. Wanda Meek for her invaluable secretarial 
assistance in preparing this manuscript. 


Over the past 13 years a series of studies on the development of 
brain, behavior, and sodalizafion in various breeds of domesH- 
cated dog have been undertaken (Fox, 1965 and 1971). This research 
was subsequently refocused on wild (undomeshcated) canids, in- 
duding the wolf, coyote, and red fox, in order to help identify 
changes in behavior and sodalization due to domestication in 
dogs (Fox, 1971b). Differences among various wild spedes, in terms 
of communication and sodal organization, correlated with be- 
havioral adaptation to a particular niche or set of ecological var- 
iables (Fox, 1975). 

These observations led to the question of the adaptability of 
domestic dogs to “revert" to the wild, to become feral and live 
independent of man. The reversible and irreversible effects of 
domesticahon might then be demonstrated. A study of feral urban 
dogs was undertaken to answer some of these questions. This 
study underlined the tragic consequences (to the dog) of irrespon- 
sible ownership, and several sodal, ecological, and public health 
hazards were demonstrated and publicized. 

Earlier studies of behavior development and sodalization of 
the dog provided the basis for a number of publications to educate 
the general public and thereby improve the relationship bctivecn 
man and dog through understanding (Fox, 1972). Following some, 
but considerably less, research on the behavior development of 


the dog: its domestication and behavior 

cats and an extensive survey of the literature, similar matenal of an 
educational nature was prepared and published for the same pur- 
pose (Fox, 1974). . , ■ , 

Research on the effects of early expenences (e.g., soaal isola- 
tion, restricted socialization) on later behavior served to establish 
some parameters for interpreting and treating abnormal behavior 
and emotional reactions in adult dogs and other domesticated ani- 
mals (Fox, 1968 and 1972). This, coupled with nationwide consulta- 
tions generated via the media (radio and television broadcasts and 
syndicated newspaper and magazine articles) and referrals of cases 
by veterinarians in private practice, produced data on a wide range 
of behavioral anomalies in pets, and often related problems in the 
pet-owner relationship. 

The phylogenetic origins of the dog, established long before 
man's intervention, are still evident today, together with the effects 
of 10,000-14,000 years of selective breeding during its period of 
domestication. As the various needs and life-styles of people 
change, so the relationship between pet and owner and pet and 
home environment changes. Such contemporary influences repre- 
sent the more dynamic and labile aspects of the process of domesti- 
cation, an understanding of which is important for the well-being 
of animal and man alike. 

Some of the more general aspects of domestication first are 
reviewed from an ethological vieivpoint and various concepts and 
principles outlined. Given the complexities of the domestication 

process and the lack of historical records, an objective study of the 
effects of domestication in any given species must be conducted at 
four levels; comparative behavioral and sodo-ecological studies of 
wild and domesticated canids; genetic studies of hybrids of wild 
and domestic spedes; sodalization and effects of early experiences; 
the development of sodal relationships in hand-raised wild and 
domesticated spedes. The strong emphasis in these studies on the 
behavior of ivild canids, which may seem irrelevant or super- 
fluous, adually provides the only template for identifying and 
analj’zing the possible effects of domestication in the dog. 
Additional aspects of behavior development relevant to the com- 
plex phenomenon of domestication are also reviewed, and some 
unexplored potentials for future improvement of livestock and pets 
alike is discussed. 


Effects of 
Domestication in 
Animals: A Review 



the dog: its domestication and behavior 

Table I. 

Under noturol conditions ^ 

1. Emergence of a new character or character complex making it possible to 
occupy previously unoccupied ecological niches. 

2. Explosive adaptive radiation into all available ecological niches (carni- 
vores, herbivores, etc.). 

3. Darwinian selection between species. 

4. Adaptive radiation within species. 

5. Increasing specialization within the ecological niche. 

6. Specialization by minor or nonadaptive (neutral) specialization. 

7. Cessation of discernible evolutionary change — highly specialized in an 
unchanging environment (e.g., horseshoe crab); extinction if unable to 
adapt to the changing environment. 

Under domestic conditions 

1. A shift in human culture provides a new ecological niche for those 
species with favorably adapted characteristics. 

2. Explosive domestication of many forms to serve human culture (scaven- 
gers, milk producers, draught animals, etc.). 

3. Darwinian selection between species. 

4. Divergence vdthin domesticated spedes toward different specialized 
functions (e.g., among dogs, cattle, etc.). 

5. Inaeasing improvement along a straight line for a behavioral function 
(increased milk production, speed, etc.). 

6. Development of breeds or varieties by nonfunctional (morphological) 
diversification and imposed reproductive isolation. 

7. Some forms apparently do not respond to further selection; the con- 
dition is likely to be transient, or the stock replaced by a line which will 
continue to respond. 

The factor of time over gencratiorrs is a vital aspect of the 
process of domestication. Domestication is an evolutionary process 
resulting from changes in the selection pressures on a species or 
population created by an artificial environment, with release from 
the competition for survival characteristic of a natural habitat (Allee 

Effects of Domestication 


E = Experiences, pre & postnatal 

G = Genetic influences (adrenal-pit; 

neoteny; pseudospec iat i on 
* I nfant i 1 i sin;dependency 

Figure i. Schema of interrelated factors in the taming and later 
domestication of a wild animal. Socialization and related 
environmentallexperiential factors and genetic selection are entailed 
in producing a domesticated phenotype. 

et at., 1949). The significance of such environmental influences are 
elaborated upon in this book. Such conditions produce changes in 
the gene structure of a population and differential reproduction of 
genotypes over generations which could result in eventual specia- 
tion. Hale (1962) compares the general evolutionary sequences in 
animals under natural and domestic conditions. (See Table I and 
Figure i.) 

History of 

Though there is little agreement over the history of domestication, 
scholarly inquiry has produced a number of interesting theories. 
Zeuner (1963), in observing the different types of social relation- 
ships between animal and man, has proposed that domestication 


the dog: its domestication and behavior 

occurred long before the economic potential of animals in agricul- 
ture was discovered. He outlines five stages of the intensity of 
domestication, which describe both present relationships between 
man and animal and the historical development of domestication. 

1. Loose contacts with free breeding. 

2. Confinement to human environment with breeding in cap- 

3. Selective breeding organized by man to obtain certain 
characteristics and occasional crossing of wild forms. 

4. Economic considerations of man leading to the planned de- 
velopment of breeds with certain desirable properties. 

5. Wild ancestors persecuted or exterminated. 

With this outline of social relationship, Zeuner (1963) de- 
veloped a probable order in which species were taken into domes- 

1. Mammals domesticated in the pre-agricultural (Mesolithic) 

a. Scavengers: dog, pig, duck. 

b. Social parasitism: reindeer, sheep, goat. 

2 . Mammals domesticated in the early agricultural (Neolithic) 

a. Crop robbers; cattle, buffalo, gaur, batteng, yak, pig. 

b. Those systematically domesticated: fowl, hyena, ostrich. 

c. Pest destroyers: cat, ferret, mongoose. 

3. Mammals subsequently domesticated primarily for transport 
and labor. 

a. Domesticated by agriculturalists in the forest zone: 

b. Domesticated by secondary nomads: camel. 

c. Domesticated by river valley civilizations: ass, onager. 

4. Various other mammals, 

a. Small rodents: rabbit (Medieval), dormouse (Roman). 

b. Experimental domestication: hyena (Egyptian), fox 
(Neolithic), gazeUe (Egyptian), ibex (Egyptian). 

c. New World species: Hama (American Indian). 

d. Pets: Mouse (modem European). 

5. Birds, fishes, and insects (not classified). 

Effects of Domestication 


Artificial Speciation 
and Adaptive Radiation 

Under any condition, natural or domestic, the major factor produc- 
ing evolutionary change is isolation of one population of a species 
from another. In the domestic situation, a population is intention- 
ally isolated by man (whereas isolation under natural conditions is 
a result of chance). Such isolation occurs on two levels. Geographic 
or reproductive isolation occurs where a topographical barrier 
prevents two populations of a species from interbreeding. This 
leads to divergent adaptation of each population to its environment 
through new phenotypic expression of the common genotype. If 
the populations are aUowed to interbreed (gene flow) after a rela- 
tively few number of generations, speciation will not occur. Should 
such gene flow be inhibited by geographic isolation for a long 
period of time (in generations), divergence might ocair to t"® ex- 
tent of making the two populations reproductive y “e, 

and hence separate species. Isolation on this level is twofold. Be- 
havioral isolation is the result of divergence of courtship-mating 
patterns between populations. Incompatibility may also result 
from divergence in the characteristic anatomies ° P°P“'^- 

tions making reproduction mechamcaUy 

tic strains are reproductively compatible with the wild counte^arts 
of their spedes. There are very few speaes of animals that are 

solely domestic. ... 

It is obvious therefore, that domestication is, as is any evolu- 
It IS , ' f intricate combination of environ- 

honary process, the 'result ofj^n inmc potentials of a 

mental influences coup ® spedfic environment, man 

spedes. Through manipulation of the spea ,Dedes to 

can accelerate the evolution of certain ° hich 

suit his spedfic needs Other enwrOTmen^a reactivity, 

may greatly modify the animal s be 

and sodabmty, wUI be discussed m Chapter 9. 


the dog: its domestication and behavior 

The Effects of 
Domestication on 


With an understanding of what domestication involves, we can 
begin to look at its various effects. There are a few major factors 
inherent in the process of domestication itself that directly influ- 
ence the behavior of a species (Fox, 1968c). The first of these is the 
change in environments from a natural habitat to the habitat 
created by man. The basic evolutionary aspects of this change al- 
ready have been discussed. An animal will respond to the type of 
domestic environment in which it is placed. An artificial environ- 
ment, depending on the specific circumstances, can have a great 
influence on the general behavior, disease resistance, and total 
productivity of the species. The average zoo, where conditions of 
captivity have many of these effects, is a good example of this. 
Different individuals and different species will adapt better to this 
type of situation than others. A simulated natural environment 
frequently is easier to adapt to and provides for a minimum of 
incidence of behavioral abnormalities and stress diseases. Man will 
create either of these domestic environments to suit his needs (Fox 
and Walls, 1973). 

The second major factor influencing behavior (Fox, 1968b) is 
the genetic selection of specific strains from a few species of ani- 
mals originally domesticated. Man selects such strains for a 
number of general characteristics. 

1. DodUty — this is a heritable trait. 

2. Adaplability and fitness for different domestic environments. 

3. Desirable characlerislics of economic importance which can be 
enhanced through breeding such as high fertility, rapid 
growth, efficient food conversion, etc. 

4. Fixed paedormorphic features which reduce the time span 
from birth to maturity, but allow a high degree of adapt- 

Effects of Domestication 


ability because of perpetuation of certain infantile charac- 

5. Reduction of wild characteristics (especially aggressive and 
sexually related display structures) such as horns, hair, etc., 
by neoteny (similar to 4 above). 

6. Hybrid vigor through crossbreeding. 

This type of direct (genetic) selection will precipitate a ar 
specialized deviation from the natural behavioral nom an 
changes in behavior patterns resulting from sirnply a c 
environment. Also, any exaggeration of certain p 
teristics through breeding will be accompanied y P 
changes in characteristic behavior. 


A number of natural behavioral stat^ 

adaptive in faciUtating transition from a wi o ^ domesti- 
Hale's (1962) observations are „.,_ricHcs listed on the 

cated species might not show all of the cha ^pc showing a 

left sid"e of this fable, but it is colfmn cof Id 

majority of the behavioral characteristics i & 

adapt to a domestic situation. 

Group Structure u„.H.ivr>e social groups with 

In a domestic situation, flock- or he j, n,ore managc- 

often well-defined dominance hierarchies structure, 

able and easily maintained than a teiritona , orcanization re- 

A loose social hierarchy or leader-follower to the 

duces the number of conflict situations a croup would have 
social stress of confinement, situations where 

a similar advantage over a terriloria to provide large 

large numbers must be housed ■ h the domestication of 

quantities of produce. (An exception to * proximity mtol- 

lerrilorial species as family pels.) A re also have 

orance (social distance) and intraspeafic « gg 
had high selection priorities in domes ica 


THE dog; its domestication and behavior 

Table 11. 

TavoraUe characteristics 

1. Group structure: 

a. Large soda! groups (Hock, herd, pack), true leadership. 

b. Hierarchical group structure. 

c. Males affiliated with female group. 

2. Sexual behavior; 

a. Promiscuous matings. 

b. Males dominant over females. 

c. Sexual signals provided by movement or posture. 

3. Parent-young interactions: 

a. Critical period in development of spedes-bond (imprinting, etc.). 

b. Female accepts other young soon after parturition or hatching. 

c. Precodal young. 

4. Responses to man: 

a. Short flight distance with man. 

b. Little disturbed by man or sudden changes in environment. 

5. Other behavioral characteristics: 

a. Omnivorous 

b. Adapt to a wide range of environmental conditions. 

c. Limited agility 

Unfmjorable characteristics 

a. Family groupings. 

b. Territorial structure. 

c. Males in separate groups. 

a. Pair-bond matings. 

b. Male must establish dominance over or appease female. 

c. Sexual signals provided by color markings or morphological structures. 

a. Spedes-bond established on basis of spedes characteristics. 

b. Young accepted on basis of spedes characteristics (e.g., color patterns). 

c. Altridal young. 

a. Extreme wariness and long flight distance. 

b. Easily disturbed by man or sudden changes in environment. 

a. Spedalized dietary habits. 

b. Require a spedfic habitat. 

c. Extreme agjlity. 

Effects of Domestication 


Sexual Behavior 

The most important adaptive trait of a species is its ability to 
reproduce under domestic conditions. Promiscuous sexual be- 
havior has obvious advantages over the establishment of pair- 
bonds in domestic situations where certain traits are being bred for, 
and sires are being used. Established male dominance over females 
reduces conflict between courtship behavior and aggression, thus 
normally facilitating mating behavior. Posture and movement as 
sexual response eliciting stimuli are more stable and adaptive and 
presumably more important than sexual display structures. The 
latter secondary sexual characteristics are less necessary for re- 
production in captivity since their reduction (through neoteny) 
does not lower reproductive success in captivity (although it would 
in the whd). Disruption of the former characteristics may directly 
affect the breeding capabilities of the species. Other social and 
developmental influences on reproductive behavior are discussed 
in Chapter 9. (See also Enders, 1945.) 

Parent-Young Interactions 

The establishment of a spedes-bond by imprinting of young 
has distinct advantages in adapting to a domestic environment 
During the critical period of imprinhng, young can be separated 
from parents in groups and raised by humans, thus alteraig t eir 
sexual preferences little and sodalizing them to man. recocia 
young have an earlier opportunity than altridal young or impnn 
ing during the critical period. Acceptance of ahen young by some 
spedes (allowing transfer of wild young and * a °P 
tates successful establishment of a speaes un er o nthpr 

tions. Recognition of young by spedes color because 

spedfic cues) is less adaptive under th«e con 1 . ^ . 

fLales might kill young of other mothers because of vanations in 
color patterns or overt behavior per se. 

""Tston n^h. distance and minimum ^isnipt^n -h the pm. 

ence of human! fadlitates handling and reanng. 

man early in life W )““ doe! imprinting to 



THE dog; rrs domestication and behavior 

cialization in wild versus domestic canids is discussed in detail in 
Chapter 8. Genetic selection for high proximity tolerance and high 
response threshold and flight distance to novel stimuli may have 
been a consequence of selection for docility (see also Beylaev and 
Trut, 1975). 

Socialization plays a key role in both the initial phase of 
domesticating a species and in maintaining domestic conditions 
with each generation. An animal must be socialized to humans 
without altering the sexual preferences of the species or causing 
rejection of the animal by its own species. Constant handling at a 
young age will socialize wild rats to humans, but the rats must be 
handled throughout their lives to maintain this tractability (Richter, 
1954). Similar "regression" in the absence of continued social con- 
tact has been noted in some foxes and coyotes, although individual 
variability is considerable. Wild adult animals may become 
habituated (or tamed) to man, but only the more sociable and gre- 
garious (e.g., wolves [Woolpy, 1968I) can become socialized (i.e., 
emotionally attached) when adult. When young, socialization is 
usually very rapid but may not endure if that species is by nature 
nongregarious or relatively asocial (see Chapter 8 for further obser- 

Table III, modified from Fox (1968b), evaluates the various 
stages involved in the socialization of animals to humans. 

Food and Habitat Characteristics 

"Ability to meet needs for food in man's environment or live 
on the byproducts of his agriculture is essential for complete 
domestication" (Hale, 1962). A flexible diet is adaptive under 
domestic conditions. 

Specialized habitat requirements are a disadvantage under 
domestic conditions as confinement prevents searching for ideal 
habitats. Thus limited agility is also adaptive. 


Eibl-Eibesfeldt (1970) views domestication as resulHng in generally 
simpler behavior. Alterations in characteristic behavior patterns 

Effects of Domestication 


under domestication are the result of the various adaptations a 

species must make to a given set of conditions. Such adaptations, 
in many cases are learned, and modification occurs in the appeti- 
tive sequences of behavior. An example of this might be a change 
in the manner a domestic animal searches for food. Pigs might 
learn that food is kept in a feeder and it can be obtained by lifting 
the cover of the feeder rather than by searching for food in a field or 
pen. New appetitive behavior leads to the species' characteristic 
consummatory response, in this case, eating behavior characteris- 
tic of pigs, as these patterns of behavior are highly stable. 

Adjustments in behavior can also result from simply learning 
to respond in characteristic ways to new stimuli associated with the 
domestic environment. Stimulation for the release of milk in dairy 
cows is frequently switched from manipulation of the udder by 
calves to the rattle of cages and equipment at milking time (Ely and 

Peterson, 1941). , . ,u 

The effects of selective breeding are readily observed m the 
more malleable behavioral traits. As has been discussed, most ^sic 
motor patterns resist modification under domestic condihons. Cer- 
tain of these patterns will combine through hybndizahon some- 
times creating difficulties because of ambivalence in the reactions 

of the hybrid. , , , j „ 

Under domestication, territorial patterns tend to 
Those species with a greater flexibility in their soaa s . , , 
generally adapt better to the domestic environmen . a 
points out, though, that some species have a . jg 

vergent social structures." Some species whose soa ^ P. . , 
based on hierarchical structure in a wild habitat ' 

under domestic conditions. Changes also occur arranee- 

habits of some species where reversion from pair-bond arrange- 
ments to promiscuous mating takes place. frpauencv 

Selecttve breeding shows a marked effect ‘he frequen^ 

and intensity of certain patterns of behavior ^ Apparent 

response thresholds necessary to eUa‘ populaHons 

elimination of certain of these patterns 1 This has been seen 

is the result of an increase of these ^eshNds. Th. has 
in experiments with a number “ SP ^t. It has been 

experimentation has been done w^h . es^cated strains of 
shown (Barnett and Stoddart, 1969) ‘hat domesnca 


the dog: its domestication and behavior 

this species have higher thresholds for aggression in a conflict situ- 
ation and are less suspicious of new objects, food, etc., as a result 
of a higher threshold for avoidance behavior and neophobia (Bar- 
nett, 1958). Keeler (1970) has shown that selective breeding for coat 
color in color-phase foxes produces higher thresholds for behavior 
associated with the fear response.* 

Because the domestic environment removes many of the selec- 
tion pressures of the natural habitat, behavior patterns adaptive to 
competition for survival are not as adaptive under domestication. 
Domestication does not remove responses of fright, aggression, 
etc., from the repertoire of behavior of a species, and occasionally 
such behavior patterns occur spontaneously as vacuum activities 
(Fox, 1968b). More usually, however, without reinforcement and 
no longer being of adaptive value, they may be easily eliminated 
through selective breeding. 

"Purely intra-specific selective breeding can lead to the de- 
velopment of forms and behaviour patterns which are not only 
nonadaptlve, but can even have adverse effects on species preser- 
vation" (Lorenz, 1968). Selection for traits of economic advantage 
to the breeder can result in disruption of the coordination of certain 
patterns of behavior unless stability of these behavioral traits is 
bred for simultaneously. This disruption has been seen in certain 
strains of turkeys bred for extreme breast size. Some males exhibit 
sexual-copulatory behavior toward piles of dirt, rarely mounting 
females. Perpetuation of these strains is accomplished by artificial 
insemination (Hale, 1962). Complete evaluation of many of these 
behavioral disruptions is complicated by the lack of adequate in- 
formation on the occurrence of such patterns in wild strains. 

Threshold changes induced by domestication have already 
been mentioned. Occasionally selection for certain behavioral traits 
leads to undesirable changes in other patterns of behavior. Certain 
strains of turkeys bred for hypersexuality have shown decreased 
thresholds for imprinting to man, resulting in the display of sexual 
behavior directed toward the caretaker! 

Another maladaptive consequence of intense selective breed- 

•In view of the marked differences within dog brecdsof individuals having different 
coat colors, a dcuilcd study of the relationship between coal color and tempera- 
ment IS needed. 

Effects of Domestication 


ing is the appearance of behavioral phenodeviants in hybrids 
which are not apparently present in either parent strain. A certain 
hybrid strain of turkey has been observed denuding many mem- 
bers of the flock spontaneously. Deviant behavior has been seen in 
mammals where in one case a hybrid strain of female mice is 
known to eat specific digits from her offspring while cleaning 
them. This phenomenon, according to Hale (1962), remains basi- 
cally unexplained. 


As man domesticates a species he is endeavouring to shift that 
species from the adaptive peak representing the natural habitat 
and ecological niche to a new adaptive peak representing the artifi- 
cial, domestic habitat. The success of this shift is primarily depen- 
dent on man's ability to maintain the reproductive fitness ot the 
species. Many species have a number of characteristics favora e to 
domesticahon, and the valley between peaks is a shaUower one 
than the transition for species with fewer favorable charactenstics. 
Occasionally, a species well adapted to the domestic environmen 
may lose some reproductive fitness during selective ree mg or 
specific specialized traits. This problem can be dea t wi y re 
ing selection for the desired trait causing some regression o 
trait, but allowing the reproductive fitness of the stram ‘o 
a new gene pool to establish itself, and thus copu a ^ ® , 

new adaptive peak. Hybrids produced from crosses ^ 

mestic and wild strains of the same species frequen y 

nations of characteristics unfavorable for succes 

either habitat. Crossbreeding between two or considerable 

domesticated animals (dogs or cattle) can hybrid 

improvement in performance — a valuable as 



THE dog; rrs domestication and behavior 

The Effects of 
Domestication on 

Changes in the environment alter the physiological needs of a 
species, and corresponding adjustments of behavior occur. Thus, it 
is important to consider physiological change as a basis for many of 
the changes in behavior due to domestication. 

The hypothalamus has been implicated in changes in the de- 
gree of characteristic aggressiveness in wild and laboratory bred 
rats. As Barnett and Stoddart (1969) have pointed out, laboratory 
bred rats are much less prone to attack or threaten a strange rat in a 
conflict situation than a wild rat which will frequently kill a 
Stranger. This "killer instinct" has been "tamed" in wild strains by 
the injection of methyl atropine into the hypothalamus and surfaced 
in domesticated strains by a similar injection of various cholinomi- 
metics. Rats are indicative of the general trend toward docility in 
domesticated animals, and the possibility of hypothalamic change as 
a cause of this is currently being researched. 

Richter's (1954) work with the Norway rat has shown that 
domesticated strains have a lower characteristic metabolic rate re- 
sulting in a lower food and water intake per kilogram of body 
weight. Coupled with this is a lower resistance to poisoning than is 
seen in wild rats. 

Nervous system changes accompany domestication. Changes 
in the frontal poles are another factor in the docility seen in domes- 
tic rats. Removal of the frontal poles causes domesticated rats to 
lose much of the savageness of wild rats (Richter, 1954). The sen- 
sitivity of various neural structures to hormones may change. 
These specific changes cause changes in both the physiological and 
behavioral thresholds of the strain (Hale, 1962). 

Beylaev and Trut (1975), in selecting for docility in successive 
generations of silver foxes, found changes in morphology, estrous 
C)-cles, and adrenal responses to stress and ACTH administration. 
They conclude that "selection for dodle, tractable behaviour leads 
to the dramatic emergence of new forms (phenotypes) and to the 

Effects of Domestication 


destablilizaKon of ontogenesis manifested by the breakdown of 
correlated systems (adrenal-pituitary, gonadal-pituitary) created 
originally under stabilizing selection." They present an important 
concept of destabilization where artificial selection can increase 
phenotypic variance and alter the wild phenotype (structurally, 
physiologically, and behaviorally) as exemplified by the domestica- 
tion of animals. 

Several of the general and theoretical issues pertaining to the 
effects of domestication are examined experimentally, with first a 
detailed analysis of the social behavior of wild versus domestic 


Socio-Ecology of Wild 
Canids: Environment 
and Behavioral 



THE dog: its domestication and behavior 

The Distribution of 
Canids , 

The domesticated dog has many cousins which belong to the fam- 
Uy Canidae (see Figure i). These include the coyote and wolf, vari- 
ous species of fox and jackal, the lirdian dhole, and the Cape hunt- 
ing dog (Staines, 1975). The doglike "foxes" of South America, 
such as the maned "wolf," bush dog, small-eared dog, crab-eating 
fox, and Culpeo are unlike any of the other canids, their unique- 
ness probably being related to the great length of time that the 
continent of South America was effectively cut off from the rest of 
the world. In contrast, the jackals of Africa and Asia more closely 
resemble the coyote of North America and, similarly, the pack- 
hunting dhole of India resembles somewhat the Cape hunting 
dog. These similarities may be interpreted as evolutionary paral- 
lelisms and convergences. For example, the coyote and golden 
jackal may not, in fact, be distantly related, but, instead, have come 
to resemble each other because of their specialization to a particular 
niche or life-style. 

In the Northern hemisphere, the wolf is widely distributed 
and may be regarded as the most successful of the pack hunters 
(the other two pack hunters being the Cape hunting dog and the 
dhole), being found as far north as the Arctic, as far south as 
Mexico, and as far east as Asia. There were many races or sub- 
species of wolf, most of which are now extinct because of man's 
invasion and exploitation of their hunting ranges and systematic 
destruction of predator species. Consequently many races of 
wolves, superbly adapted to particular regions after generations of 
evolution, are now extinct. Similarly, the red wolf {Canis nigerl 
nifus), once abundant in Texas and Florida, is now virtually extinct. 
A few specimens still remain in the Texas gulf area, many of which 
have been crossbred with more tenacious coyotes, so that few, if 
any, red wolves are left. 

The other two species of pack hunting canids are also facing 
possible extinction. Until it was realized that predation by Cape 
hunting dogs was beneficial to quality and population control of 
hoofed animals in Africa, the dogs were shot on sight. (In some 
areas they are still shot for "disturbing" the herds of big game!) In 

Socio-Ecology of Wild Canids 


Vulpes spp. 













C. lupus 

/[ C. forniliaris 

I C. rufus 

\ aureus 



C. latrons 

Figure 1 . Schema of taxonomic relationships 

based upon behavioral evidence ili.irrs and other 

mon origin of uvif (C. lupus) and dog (C. • nnor to 

uvtflike canids), probably differentiating as separ ./ 

mafi'5 domestication of the dog. 


THE dog: its domestication and behavior 

India, the dhole is in a similarly precarious position, as are many of 
the carnivores (see Fox, 1978). 

In contrast, the more solitary predators, such as the red fox 
and coyote, are more adaptable to human intrusion and predation. 
The elusive coyote numbers at least 40,000 in Kansas alone, while 
in England, there is a high fox population in Tilbury docks, which 
competes with the indigenous warehouse cats for rats and garbage. 

The raccoonlike dog from Japan, which in the fall becomes 
very fat and may hibernate in the winter, is another example of a 
successful canid. Imported to Finland for commercial fur produc- 
tion, it escaped from the ranches and is now wild in many Euro- 
pean countries including Poland and Czechoslovakia. The dingo of 
Australia, which closely resembles the smaller dogs of New Guinea 
and Malaysia, was originally a domesticated dog brought into the 
continent by early aboriginal settlers. It has since gone wild, be- 
coming well established as the main predator because there were 
no other placental carnivores with which to compete (Macintosh, 


Having briefly considered the distribution of canids, we will 
now look at their behavior. The comparative analysis of social or- 
ganization and communication signals can give us some insight 
into the evolution of social behavior within a family of related 
species. Similarly, comparative studies of the same species in dif- 
ferent habitats show how such a species has adapted socially and 
physically to a particular set of environmental conditions (e.g., 
distribution, abundance, and type of prey) and differences in ter- 
rain (mountain, tundra, or open prairie). 

Communication and 
Social Organization 

The canid family comprises an assembly of species that span the 
entire spectrum from the relatively solitary red fox to the gregari- 
ous wolf. Consequently, this family provides a valuable research 
opportunity for studying the evolution of communication 
mechanisms in related species differing in social behavior and in 

Socio-Ecology of Wild Canids 


the sodo-ecological patterns or life-styles that they have evolved. 
The relatively solitary canids such as the red fox have a simple 
repertoire of visual signals — tail and body positions and facial ex- 
pressions. Similar basic signals which serve to increase, decrease, 
or maintain a certain social distance or proximity are recognizable 
in the more social canids, but in these species, the signals are more 
variable and are subtly graded in intensity. Greater complexity of 
signals and, therefore, greater message carrying potential is also 
afforded by rapid successive and simultaneous combinations of 
these signals. Thus, the wolf and domesticated dog can give suc- 
cessive alternate signals of submission and defensive aggression or 
can combine, simultaneously, signals of submission and greeting. 
Very similar signals are present in the less social canids, but they 
often appear at a "typical intensity" and lack these more subtle 
intensity shifts. The threat gape of a red fox is very much an all or 
nothing signal, while the wolf has a greater repertoire of threat 
signaling (Fox, 1971b). 

These generalizations may point to the fact that with increas- 
ing sociability and sustained proximity, a strong selection priority 
was placed upon the development of more sophisticated visual 

Marler and Hamilton (1966) have pointed out that the more 
solitary primates have highly stereotyped calls, while the more 
sociable species have more subtle and variable vocal patterns. A 
similar generalization may be applied to the canids, the more soli- 
tary of which have elaborate and stereotyped calls which are used 
especially during the breeding season to locate a mate and to drive 
off rivals. The more solitary the spedes (which also tend to be 
nocturnal), the greater is the reliance and priority upon auditory 
communication because visual signals are ineffectual when indi- 
viduals are separated by some distance. Wolves and coyotes also 
have distance-communication signals; their hoivis, interspersed 
with barks and yips, serving to bring companions together and 
possibly to inform rival individuals or packs of their presence. The 
more solitary canids apparently have not evolved a howl in their 
vocal repertoire, so that the howl seems to be correlated with more 
complex social interaction (see also Chapter 4). Wolves and Cape 
hunting dogs often engage in a mutual greeting and singing (or 
howling) ceremony before they go out to hunt; such group K- 



haviormay serve as a pep rally, bringing all individuals to the same 
degree of excitement. 

The more solitary canids also seem to rely a great deal upon 
olfactory communication. Odors (pheromones), when deposited 
on the ground in urine or feces or against particular objects or 
"scent posts," tend to persist for a long time. The message is, 
therefore, a rnuch more permanent kind of signal and is effective 
long after the animal has moved on. Social canids mark out their 
territories and, like howling, it may serve to inform others of their 
presence and of their movements in the hunting range which others 
might use. It would seem logical that the less social canids rely 
more upon olfactory communication than the more gregarious 
species, and this is partly supported by the simple observation that 
the more solitary species smell much stronger than the more social 
ones. They are more likely to urinate or defecate on a novel odor (of 
carrion or deer musk), while the more social canids will often roll 
on such odors, their reward possibly being a lot of social investiga- 
tion when they join up with their companions later (Fox, personal 
observations). Olfactory, as well as auditory, communication would 
be essential in order for the male to locate a receptive female during 
the breeding season. In the more social canids, where the receptive 
female is always with her mate or always with the pack, the selection 
pressures for effective olfactory and auditory commurucation would 
be relaxed. 



The communication patterns are related to the type of social or- 
ganization that the various canids have evolved, which in turn 
reflects the ecological factors to which each species has adapted or 
has been shaped by. These ecological factors include primarily the 
species size, annual and seasonal distrlbutiorv, and abundance of 
prey. The type of terrain, climate, and seasonal variation in tem- 
perature are also significant, as well as the presence of other pred- 

Socio-Ecology of Wild Canids 



Bod/ Size I 

Timing of ^Motu/ity at birth^Porent-infont * 
Breeding Seoson^ Utter size 

Sociof Distance ^Signois 


(proximity tolerance) 

Figure 2. Schema of interrelated genetic and environmental var- 
iables which determine genotxfpicfphenotypic characteristics in the 
socio-ecology of canids (from Fox, 1975). Human intervention, as 
in domestication, can clearly influence these interrelationships at 
almost every interphase, leading to increasing genotypic destabiliza- 
tion and phenotypic variance in such variables as proximity tol- 
erance, temperament, body size, and reproduction. 

ators of greater or lesser size which occupy competitive or non- 
competitive niches in the same habitat. 

Competitive ruches are rare and when competition between 
predators occurs, the ecological balance may be disturbed. Where 
there is an abundance of many different prey species ranging 
greatly in size, a greater diversity of predators can be supported. 
Thus, wolf, coyote, and red fox, or Cape hunting dog, golden 
jackal, and bat-eared fox may be found in the same habitat, each in 
its own particular niche and each occasionally scavenging on the 
remains of a kill made by a larger predator/ Indirectly, one pred- 
ator may assist another in the complex food chain by regulating 
population growth and preventing starvation. For example, 
smaller predators that specialize on small herbivorous mammals 
(rabbits and rodents) prevent the latter from becoming too abun- 
dant which, if they did, would lead to overgrazing which could 

’Interestingly, and tragically, the extermination of the wolf in . 

resulted in a decline in the wolverine, Arctic fox, owl, and raven, an 

that relied greatly on the remains of wolf kiUs as their pnme source of food 


THE dog; its domestication and behavior 

cause infertility, starvation, and death of larger herbivores such as 
deer. The larger predators that depend on the latter would then 

The equilibrium maintained between prey and predator popu- 
lations is remarkable, the complexities of which are only just be- 
ginning to be understood. Wolf packs in Alaska and Isle Royale 
have remained more or less the same size over the past 30 years, 
and even in years when prey is abundant, the pack size does not 
suddenly increase (Haber, personal communication). Many of the 
factors which regulate pack size remain to be identified, but some 
have been detailed (Fox, 1973 and Fox effl/., 1974). In most canids, the 
breeding season is timed so that the birth of young will coincide 
with the birth of prey species, at which time food is most plentiful. 
The prey tend to give birth all at the same lime, such reproductive 
and parturient synchrony possibly enhancing survival because the 
predators would eat their fill and be satisfied. If the birth of young 
were not synchronized but instead extended over a longer period, 
predators would take a far greater toll on the newborn before the 
latter were able to fend for themselves. 

Social Organization 

Theie are three basic patterns of social organization in the Canidae. 
In Type I, such as the red fox, only a temporary bond is formed 
during the breeding season between male and female (Burrows, 
1968). The male may stay with the female and assist in providing 
food for the young, but the Utter is usually deserted by the parents 
around 4-5 months of age. No stable hierarchy or peck order de- 
velops in the litter, so that, in the absence of strong social bonds 
and other group-cohesive forces such as leader-follower relation- 
ships, the litter breaks up and individuals go their separate ways as 
solitary hunters. 

In the Type II canid, such as the coyote (Gier, 1975) and golden 
jackal (Van Lawick and Van Lawick Goodall, 1971), there is a more 
or less permanent pair-bond between male and female, and their 
offspring may remain with them until the following breeding sea- 
son. They may then be driven out of the parents' territory, but 
occasionally when there is an abundance of food, and therefore 

Socio-Ecology of Wild Canids 


reduced competition, some yearlings may stay and even assist the 
parents in tending for the next batch of offspring. Such occurrences 
are rare. More usually the litter disperses, and each member seeks 
its own fortune outside of its natal territory. How early familial 
relationships influence later social interactions between Type II 
canids sharing the same hunting range remain to be evaluated. 

The most detailed studies of the sociai dynamics in Type III 
canids have been done on the wolf (Mech, 1970). There is stiil some 
doubt about the origin of the pack, but the general consensus is 
that the pack consists of related individuals of various ages. There 
is a binding leader-follower relationship between subordinate 
wolves and the lead or alpha wolf. A dominance order is seen 
among the females and the males, the alpha, or most dominant 
male, serving not only as a leader and decision-maker but also as a 
"policeman” who often intervenes to settle disputes that flare up in 
the ranks. There are pack rituals that may serve to maintain and 
reinforce social bonds; subordinates will affectionately and submis- 

sively greet and mob the leader, while the leader may present 
the pack with some token food object. Pack members will assist a 
mated pair in feeding the young and in guarding them when the 
pack is away on a hunt. As the young mature, they may be re- 
cruited into the adult pack and essentially fill vacant places af- 
forded by the death or departure of others. If such vac^cies are 
not available and food is scarce, mortalities will be high. Occasion- 
ally such a large pack may spUt up and the yourig, their parents, 
and one or two other adults may move into a different hunting 
range or remain in the same locale while another segment of the 
pack moves out. Such emigrations would on^ be possib e where 
neighboring packs are not in posession of adjacent temtory an 
hunbng range. The factors which reflate pack size over genera- 
tions of offspring remain to be idenhfied. It is known at 
every adult in the pack does not breed and that there is a kind of 
socid control of breeding.* Usually 
breeds; she subordinates other femaks and 

show any overt sexual behavior to the mate of he choice (nhich 
may or may not be the alpha male) or to other males. 

•Group vocrlizations in wolves and coyotes may have some 
cpidcictic function) to regulate reproduction 

Figure yhlerspcdes differmcc in mlraspecirw aggression 
Coyote cabs are extremely aggressive while Jlf ente of the a 
age engage m sustained bouts of play. Tacing page: At a lal 

Socio-Ecology of Wild Canids 



THE dog: its domestication and behavior 

Temperament and 

What determines whether or not a young fox or wolf cub will live a 
solitary or group-oriented life? It seems that much is determined by 
the basic temperament of the species, as well as by the presence or 
absence of the group-cohesive forces alluded to earlier. We might 
postulate that a socal drive independent of a sexual drive in the 
Type H and Type HI canids keeps individuals together outside of 
the breeding season. Recent research on young wolf, coyote, and 
red fox cubs supports the notion that temperament is also a major 
determining factor (Fox, 1975). Young foxes, from an early age, 
show great proximity intolerance; each one is an individual and 
each is invariably very confident, inquisitive, and highly efficient at 
killing prey. In wolf litters, there is a much greater range in indi- 
vidual temperaments, ranging from the shy, timid type (who are 
often too afraid to attack small prey) who tend to be the subordi- 
nates to the confident and outgoing type. The latter are the domi- 
nant wolves who are very inquisitive and kill prey at an early age. 
They also act as leaders or initiators for their less outgoing litter- 
mates. Such a spectrum of individual differences, coupled with 
group-coordinated behavior, social facilitation of actions, and a 
strong tendency to follow the leader, insures pack formation. 

There may be a strong selection primarily for such hetero- 
geneity of temperaments (behavioral polymorphism) within wolf 
Utters, while in the Type I canid, selection has been for a greater 
homogeneity of temperament. Litters of coyotes so far studied, 
as would be anticipated, lie somewhere between the red fox 
and the wolf in that they show considerable proximity intolerance 
and aggression toward each other, have little group-coordinated 
^havior and leader-follower tendencies, but are capable of form- 
ing a fairly stable dominance hierarchy. 

Socio-Ecology of Wild Canids 


Development of 
Aggression and Social 

Wolf cubs begin to play around 3 weeks of age, and their bites, 
unlike coyotes and foxes, are gentle and controlled. They rarely 
fight — usually to establish dominance relationships around 5-8 
weeks of age, especially in those individuals having similar outgo- 
ing temperaments. In contrast, the fox species, and coyotes and 
jackals, are very aggressive, and fighting often occurs before they 
actually engage in play. At 3 weeks of age the bite is not as inhib- 
ited as in the wolf, and they seem to have to leam to control it (Fox, 

When first put together, domestic dog pups that have been 
raised apart from each other in social isolation until 12 weeks of age 
play for only brief periods. Play bouts are broken by one biting its 
partner too hard. After 3-4 days, though, play bouts are more 
sustained because they have now learned to control the bite. 
Therefore, social experience, as well as genetic influences, contrib- 

utes to the control of bite intensity. 

Social relationships are based primarily upon who is domi- 
nant, and dominance relationships are usually firmly established in 
coyotes and jackals by 4-5 weeks of age. By this age, they are more 
likely to play, the subordinates often showing more play-solicitmg 
than their more aggressive littermales. 

Foxes, although very playful by this age, do not forrn close 
affecHonal Hes with each other, and play often ends m a fight. Fox 
cubs rarely engage in group activiHes-each one is a confident indi- 
vidualist. Their egocentric temperaments (high ' 

erance) and loose social ties in infanc>- suit them ivell to 
tary life; by 5 months the litter splits up each one going it.s ou n 
separate way The parents usually leave the young and at this time 
the bond bL-een the parents is also broken. [Occasionally the 
bond may break after mating, and the vixen raises the cubs herself 

‘’’“"in conirat/tL the fox, a litter of wolf cubs has a greater range of 


the dog: its domestication and behavior 

temperaments. One or two are dominant and outgoing leaders, 
others are followers, and some are very timid and dependent. Es- 
kimo hunters state that some wolves never kill prey— perhaps 
these belong to the latter category. Research on several litters of 
wolf cubs at the Naval Arctic Research Laboratory at Point Barrow, 
Alaska has confirmed this polymorphic heterogeneity of tempera- 
ments in wolf litters (in contrast to the monomorphic temperament 
of more homogeneous fox litters [Fox, 1975]). This phenomenon in 
wolf litters may facilitate pack formation; all cannot be leaders and 
there must be followers. A greater range of temperaments would 
facilitate division of labor, of activities or roles in a social group 
comprised of individuals of different rank, sex, age, and having 
different temperaments and allegiances. Dr. David Mech (personal 
communication) has been studying several packs of wolves marked 
with radio collars in Minnesota and has also tracked several loner 
wolves. These are not all old outcasts or low-ranking youngsters; 
some seem to be young dominant wolves that simply cannot inte- 
grate with the pack in which there is a firmly entrenched leader. 

Fox and Andrews (1973) have recently found significant 
physiological differences, as well as behavioral differences, in wolf 
cubs of high, low, and Intermediate rank. High-ranking wolf cubs 
and yearlings have a greater sympathetic tone (higher resting heart 
rates) and are both behaviorally and physiologically more active 
than subordinates. These physiological differences discovered in 
wolf cubs may be the basis for differences in temperament or per- 
sonality. It remains to be seen if, when a wolf experiences a change 
in rank, there is concorrritant physiological change. For example, 
would a low-rankmg cub with a low resting heart rate have a 
higher heart rate if it experienced an elevation in rank? Candland d 
al . (1970) did find that heart rate changes with a change in social 
rank in groups of chickens and squirrel monkeys. 

Foxes together in captivity show little group-coordinated activ- 
ity and do not follow a leader like the wolf. This innate tendency to 
follow may be a major reason why wolf cubs stay in a pack. 
Another reason may be the maintained responsiveness of wolf 
cubs to their parents (and vice versa). Fox and coyote cubs show a 
decreasing responsiveness to their parents as they mature, while 
wolf cubs continue to be highly responsive. A transference may 
occur where the young wolf reacts to the leader (which may or may 

Socio-Ecology of Wild Canids 


not be a parent) in the same way in which it behaved toward the 
parent as a cub. 

The temperaments of young foxes and wolves seem well fitted 
to their particular life-styles. If foxes were to hunt in packs, one 
mouse or rabbit would not go far. Since their major prey is small 
and widely dispersed, their temperament and solitary method of 
predation are superbly adapted to their particular ecological niche. 
Wolves, in contrast, cooperate in hunting and are able to transcend 
their body size limitation by cooperating to secure prey many times 
larger than themselves. Wolves that prey mainly on deer tend to be 
smaller in size and in smaller packs than other races that hunt 
moose, for example. When food is scarce, the wolf pack will tem- 
porarily split up, and in some areas where food is scarce, as in 
Mexico, wolves are rarely seen in packs. In Italy, they do not hunt 
in packs but are mainly solitary village scavengers (Zimen, per- 
sonal communication). Such regional ecological differences have 
contributed to the evolution of various races of wolves. 

The coyotes represent a canid type intermediate between the 
fox and the wolf. They neither form permanent packs nor live a 
relatively solitary existence but instead tend to maintain a perma- 
nent pair-bond. Litters of coyotes show a greater range of temper- 
ament than the red fox but less variants than in the wolf, i.e., 
oligomorphic. They do not disperse until around ii months of age 
(i.e., around the time that the parents come into breeding condi- 
tion). Again, their temperament, greater proximity intolerance for 
each other, and relative lack of group-coordinated and leader- 
focused behavior compared to the wolf accords well with their 
social ecology. They hunt mainly small prey (rabbits, small ungu- 
lates) and usuaUy cooperate in pairs. Occasionally when there is an 
abundance of food, the young, or some of the ^ter, may s‘ay ™th 
the parents and help them rear another lifter. is is a 
type^of social behavior more typical of the wolf and has also been 
reported by the Van Lawicks (1971) i" the golden 
and jackals under certain ecological conditmns may there ore show 
some of the social patterns of wolves. This 
capacities are more flexible than in the re y' L ' -Uservi- 
food is abundant, still tends torvard a solitary li e. “^.va 

tions warrant further experimenlaHon to 
social (experienHal) determinants of behavioral adaptation 


THE dog: rrs domestication and behavior 

ecology. It would seem that the fox is genetically limited to one par- 
ticular life-style and ecological niche, while the coyote and wolf are 
more flexible. Kummer (1971), in his field studies of various races 
and subspecies of baboons, poses the same question. 

In conclusion, the red fox, coyote, and wolf represent three 
basic canid types; Type I, solitary, with temporary pair-bond; Type 
II, permanent pair-bond, with longer interaction with offspring; 
Type III, pack-forming, with strong allegiances and pack affilia- 
tions and with dominance hierarchies in both male and female 
ranks. Under certain sets of ecological conditions, the Type II canid 
may show some of the patterns of Type III, while Type III may 
adopt a Type II pattern as exemplified by the Mexican and Italian 

It is not too premature at this stage to hypothesize that temp- 
erament seems to be strongly correlated with the ecology and life- 
style of the individual and that past social and ecological factors are 
responsible for the selection and continuation of temperament 
types in the various wild canid species. Relaxation of such selection 
factors in domestication might therefore lead to greater variations 
in species-typical temperaments;’ some breeds of dog resemble 
foxes, coyotes, or alpha wolves (e.g., nongregarious, aggressive 
terriers), while others are more like middle- and low-ranking 
"omega" wolves (e.g., gregarious beagles, often lacking any social 
dominance hierarchy). 


The origin(s) of the domesticated dog and the various breeds is 
unknown (Fox and Bekoff, 1975). There may be wolf and even 
coyote and jackal ancestry (or perhaps these bloodlines are only in 
some breeds)— these three wild species all will produce fertile hy- 
brids when bred with domesticated dogs (Gray, 1954, and Koleno- 
sky, 1971). These may have been added to the genetic diversity 
wrought by 10,000 years of domesticating a dingolike dog ancestor. 
Certainly the range, variation of size, temperament, and specialist 

•Which U..ids to Lon-nz's now ui:.inlcd view of separate and wolf ancestry for 
”Dnc*m.innish" and greganous breeds of dog, respectively. 

Socio-Ecology of Wild Canids 


abilities of the various contemporary breeds is an incredible 
example of what can be done under intensive artificial selection. To 
see a naive sheep dog pup playing with a companion and showing 
all the basic actions of sheepherding, including blocking, turning, 
and driving is a dramatic case of genetic engineering. Certain 
behaviors seem to be at a lower threshold and are more easily 
elicited in some breeds than in others (e.g., herding, retrieving), 
and they are therefore easier to reinforce in training the dog. Other 
actions have a greater amplitude or intensity in some breeds; the 
pointing of bird dogs, for example, is more exaggerated than in 
terriers, while the action to attack or chase has been truncated in 
pointers (at the juncture of “orientation" in the temporal se- 
quence). Terriers show a strong tendency to seek out (i.e., 
appetitive drive) suitable objects to chase or attack, whereas a 
sheep dog may guard the same object. These are examples of 
instinct enhancement which has led to various breeds of dog 

fulfilling particular roles for man. 

The dog differs greatly from other wild canids, not in overt 
behavior per se, but in its vocal repertoire (see Chapter 4) and also 
in its sexual and social behavior. In order to successfully breed 
many dogs, the trait of monogamy or specific mate preference 
evident in wild canids has been almost eliminated. A desirable stud 
dog that is only attracted to one particular female would be of little 
value, and vice versa. Some dogs sHIl show this ancestral trait 
(Beach and LeBoeuf, 1967); female beagles and Boston temers, for 
example, if given the opportunity, have been known to accept only 

certain males. . . , 

Wild canids only have one breeding season per year, which is 
Hmed so that there will be an abundance of prey for the young 
Domestic dogs, with the excepHon of the Basenp (which has a 
photoperiodically controlled single annual estrus IScott and F , 
1965]), have two and sometimes three heats per year, ‘'•'’d h s trait 
is inherited. Artificial selecHon for this trad y/"] 

hance production. ^;°“|his js^inLTd the case in the 

domTslrc d^g T^t: nstxJ;. matS - early as 6 months, in 
uuiiie&iiL uug. ati Here a combination of 

contrast to 2 years in the woU and coy invnivpd Male 

genetic selection and improved nutntion "’fy ^ J 
wild canids produce little or no spe^ Although th,? 

season, while domesticated dogs are always potent. Although th,. 


THE dog: its domestication and behavior 

again enhances productivity, it can become a serious social prob- 
lem (see Chapter u). Dogs, then, selectively bred for utilitanan 
purposes are sexually promiscuous, precocious, and prepotent, 
and such activities can be afforded since the natural ecological re- 
straints no longer operate. 

Experiences with hand-raised canids have shown that coyotes 
and wolves, especially, become increasingly fearful of strange ob- 
jects or to a change in their familiar environment around 4“5 
months of age. In the wild, this environmental fear may be a con- 
sequence of exposure learning (or imprinting to the home range). 
It would be highly adaptive for a young animal to recognize any 
change in its familiar territory which could mean danger. In con- 
trast, the dog does not normally manifest such behavior, presum- 
ably because in the protective domestic environment which is con- 
stantly changing, such behavior would no longer be adaptive and 
would make such dogs difficult to handle as well as interfering 
with performance. An analogous fear of strangers and the capacity 
to develop sodal relationships later in life will be discussed in 
Chapter 8. 

Wolf cubs show a greater tendency than coyotes to maintain 
the infant attachment in that they invariably remain bonded to 
their human "parent" throughout life. Wolves also seem to have a 
greater capacity to develop secondary social relationships with 
strange people later in life than other wild canids, but this social 
potential is still much less than in the dog. The parent bond in the 
wolf may be transmuted to a leader bond as the wolf cub matures. 
A similar transition occurs under normal conditions in the relation- 
ship between a dog and its master as the former matures. Less 
gregarious carnivores, such as foxes, which are relatively solitary in 
the wild and break away from their parents, also will grow away 
from their human foster parents; the infant bond is not often trans- 
ferred into a social bond (leader-follower relationship) with ma- 

Domestic dogs may well have originated from a packtype an- 
cestor, since their socialization patterns are closer to the Type III 
canid than the Type I or II forms. Studies of feral urban and rural 
dogs (see Chapter 3) reveal their capacity to form packs under 
optimal environmental conditions, again supporting the view of a 
Type III ancestry. Because of suboptimal environmental condi- 

Socio-Ecology of Wild Canids 


tions, pack formation is not possible for the dingo. In this species, 
presumably, unidirectional selection over generations of feral liv- 
ing has resulted in a temperament and social organization of the 
Type II category (Corbett and Newsome, 1975). Dogs, like wolves, 
also respond to a leader in adulthood, and this tendency is easily 
transferred into the home environment where the dog becomes a 
part of the household "pack" and is ideally subordinate to the 
master of the house. But this is not always the case, and some of 
the problems of socially maladjusted delinquent dogs are discussed 

in Chapter 11. 

In summary, a lot can be gleaned from studies of wild canids 
in attempting to elucidate what effects domestication has had on 
the dog. This brings us to an important variable, namely, the pro- 
cess of socialization and critical and sensitive periods in develop- 
ment, Some analogies will be subsequently made between the in- 
terpersonal relationships of pet and owner and child and parent 
(e.g., overdependent, overpermissive) which may give rise to a 
variety of very similar emotional disorders in both dog and child. 

Behavior patterns and communication signals in these canids 
are inherited (in that they develop independent of social expen- 
ence early in Ufe). Evidence has been presented here to support the 
notion that the inheritance of certain temperament charactenstics 
or traits (which are most adaptive to a particular life-style or ecolog- 
ical niche) determines whether the animal will be sohtary or gre- 
garious as an adult. Socialization during early e a so con “ 
significantly to the formation of family bonds. In other words, by 
applying pLsonality theory and developmental 
ethology Ld ecology of canids, a more complete picmre of their 
behavifr in relation to the environment can be drawn A know, 
edge of the natural history, social behavior and development o 
each species is an essential prerequisite, and lUs unfortunate tha 
only a few studies have so far been comp e e . pnvi- 

In conclusion then, the truism that the f Xck 

ronment is confirmed in terms of to a particu- 

determine sociability, temperament, an a ap ty selection 
lar prey-predator domesHc environ- 

pressures under “"dihons of rap parricular physical 

rL^tra :n7;:y:hScaSshasoccum^^ in the domesHcated 


THE dog: its domestication and behavior 

dog. To understand what changes have occurred in the behavior 
and psychology of Canis familiaris, the variables of human influence 
must be considered. These are discussed subsequently in Chapter 
u. At this stage, some preliminary comparisons between wild and 
domesticated canids are made in relation to undesirable wild traits 
and desirable traits associated with sexuality, reproduction, and 
socialization (see Table I). 


Differences in behavior, including patterns of communication, so- 
cial organization, interpersonal relationships, and hunting be- 
havior in various canids are described. Also species differences in 
the development of aggression and the significance of individual 
differences in temperament are detailed. These behavioral dif- 
ferences between members of the canid family reveal evolutionary 
changes related to adaptation to a particular set of environmental 
conditions. Eco-spedaUzation, or socio-ecological adaptation, to a 
particular niche is manifest by a particular life-style and typologically 
distinct array of behavioral characteristics (temperament). These 
findings are relevant not only to understanding the evolution of 
ecologically adaptive behavior patterns, but they also provide a 
basis for interpreting some of the behavioral consequences of 
domestication in dogs, where both genetic and environmental 
changes have been effected by man. 


Behavior and Ecology 
of an Urban Feral Dog 


Much research has been done on the behavior geneHcs, ontogeny/ 
and ethology of the domestic ‘JogCams/amdians (Scott and FuUer, 
1965; Fox, i%a, r97«). Most ethological th ' 

taken in capHve conditions, and the question anses as o what the 
noi^al envLnment for studying the domeshc dog reaUy is^ Afer 
approximately 10,000 years of domestication, the dog shU retains 
th^e capacity to become feral. 'Boreas many dogs are conf^ne^ in 
the home, others have free access to the 

or urban. These are designated as elves 

from those feral dogs that have no hom^e and^support^he^m^^ 

Independent of human ^^^n commer^l dog food 

though, people will put assortment of feral and 

for what ‘hey f and Nesbitt (1975) have studied 

free-roaming ‘Jeg®’ environments, respectively, 

both ecotypes in urban a ter focuses on the behavioral 

The study d-^cussed m this ^ 

ecology of a tno of feral dog P L^uis Missouri, a city of 

in an economically depressed area of Sb^Lo^^^ . 

some 600,000 inhabitants, b 

""®?n several areas of the city, feral dogs were 

THE dog: its domestication and behavior 

Figure la. Typical free-roaming feral urban dogs: (A) using avail- 
able environmental resources, (B, C, and D) showing varying de- 
grees of emaciation and disease, (D) being in a terminal state. 

seen, many of which, by virtue of their condition and behavior, 
were easily distinguished from free-roaming dogs. The latter were 
usually in good physical condition, tolerated proximity of strangers 
up to 4.5-6 m (15-20 ft), and when approached further would run- 
off and seek refuge in their open backyards which were usually no 
more than 91 m (no yd) away (see Figures la and ib). From the 
security of their presumed home sites they would bark at the inves- 
tigators. Feral dogs showed a much greater flight distance, were 
more elusive and harder to follow. Sometimes they were flushed 
out of abandoned buildings which showed signs of canid occu- 
pancy (feces, shed hair on old mattresses and carpeting, chewed 
food cans and cartons and toys, such as a chewed ball or stick). 
Putrefying and mummified carcasses of dogs were also found in 
some of these buildings. The physical signs characteristic of many 
feral dogs were emadation and skin lesions (probably mange); 
some were in such poor condition that they were unable to run 

Behavior and Ecology of an Urban Feral Dog 


Figure lb. Tree-roaming house dogs: M and C) 

bage, and (B) leaving home territory for early m g f . ■ 

and social interaction in neighborhood 


the dog: its domestication and behavior 

away when first located. One was seen in the company of three 
free-roaming dogs and over a period of 6 weeks became weaker, 
more emaciated, and the skin lesions more extensive until it even- 
tually succumbed. Of course many of the dogs initially seen could 
not be classified into feral or free-roaming until we concentrated 
the study on one particular neighborhood. The neighborhood cho- 
sen was determined by the fortuitous discovery of a group of three 
feral dogs that were spotted one morning and followed into an 
abandoned house in which dog signs (feces, hair, play objects) 
indicated that they had been there for several months. 

Materials and 

The study began in late March, 1973, becoming most concentrated 
from May through July, with sporadic observations through Feb- 
ruary, 1974. Most observations were done from an automobile 
since the subjects were wary of pedestrians, and any attempt to 
follow them on foot evoked the flight response. After 2 weeks, the 
three feral dogs would allow closer proximity while the observers 
remained in the car and would walk within 0.6 m (2 ft) of the car 
when we were parked. They soon became habituated to our follow- 
ing them provided we kept the car at a distance of 6-9 m (20-30 ft). 

The pack, or trio, consisted of one tan shorthaired female 
mongrel (f) approximately 16 kg (35 lb) weight. She had elongated 
teats, a sign of repeated litters, and she was probably the oldest 
dog of the trio. The other two dogs were male, one a yellow Ger- 
man shepherd (Alsatian) (Y), weighing approximately 32 kg (70 
lb), and the other a large mongrel (X), with medium-long brindle 
hair, weighing approximately 29 kg (65 lb). The latter had a perma- 
nent hip injury, causing intermittent lameness in the right hind 
leg. All of the dogs were obviously mature (see Figure 2). All were 
in poor physical condition at the inception of the study, the 
shepherd being the most healthy of the three. The other two had 
extensive skin lesions, probably mange infestations, but by July, all 

Behavior and Ecology of an Urban Feral Dog 


three were dear and their general condition much improved (pos- 
sibly a benefidal effect of sunlight). Fecal analysis revealed heavy 
infestations of hookworm {Ancylostoma and Uncinaria) and whip- 
worm {Trichiuris). Although tempted, the observers provided no 
food or medication and in no way interacted with these animals 

during the course of the study. 

Two, and often three, observers followed the animals on 4- to 
6-hr shifts. A total of 90 hr of observation were completed, cover- 
ing all periods of the day and night. The following data were col- 

1. Daily Cycle of Activity. The time of day when active in the 
area of study, either foraging in alleys, traveling, resting in t e 
open, or hunting in the park was recorded. Much time dunng 
dayUght hours was spent in one of two abandoned house^Later m 
the summer the cool basement of one was Referred. TOe ot er 
house, an upstairs apartment, had a conveniently si a e sma 
dog door cut into the back door; the leather flap falcated when 
one or more of the dogs was in or out of the house by being tucke 

■"°2°“population Activity Index. Head counts were made at 

various hours of day and night of free-roaming og could 

of the trio's home range. This provided an 

be compared with the acHvity patterns of 'he ^ Pa^l^ '^^ich 

might, for various reasons (see ^scussiot), e movement 

3. Movements and Home Range. The range and movement 

patterns of the trio were plotted on a survey P , context 

4. Marking Behavior. The anther m^ember of the 

(presence of strange dog or marking aft Crraoinc after 

Wo had marked, i e., marking over) were recorded. Scraping 

marking was also noted. . |cad at 

5. Leadership. As the trio traveled, the one to take 

intersections and road crossings was ^^,cre made as 

6 . Miscellaneous Social Interactions. NoUations ^ 

to the frequency and type of "’‘^.”‘^*’‘’')^j‘hcirhood residents and 
riveen them and other free-roaming neighborhood 

feral dogs that occasionally came ■ openness and sta- 

7. Pack Cohesion (Fission and Fusi | . among the three 

bility of the group of interindividual relationsh p. 

Figure 2. (a) Y leaving "flaphauee"; (b) F and X following him; 
(c) Y from basement of seeand house; (d) trio crossine 

busy highway at S:is a.m. after park "hunt". Facing page- 

c and/). /cma/c F marAs in part, X marSLr; am 

Ig) tno resting in the open near second house. ,2:30 a.m. 

Behavior and Ecology of an Urban Feral Dog 


dogs were determined by (a) recording often other 

member left the group and for how long, and (b) 

dogs joined the trio and for how long. engaged primarily 

8. Hunting Behavior. In the park, the g g S ^ ^ 

in chasing squLels. The number of observed chases was recorded 

and their hunting strategy s^died 

9. Other Dog Groups. In addition to We n 

quency of occurrence of dogs egariousness of free- 

corded. This would give an index of th gr g lead to 

roaming dogs and would possibly disclose what factors 

ssss™ «... i" 

.973 10 lesl Ihe poss.bai.y of dituiol go to the parh- A‘ 

m the early part of this study the dog u^mes 1-2 hr earlier 

this Hme, they would return to one of their homes 

than during the summer schedule. 


THE dog: its domestication and behavior 



In late spring, the trio emerged from their sleeping quarters (usu- 
ally the second floor flaphouse, i.e., the house with the leather flap 
covering the cut in the door) between 11:15 p.m. and 12:00 a.m. and 
remained active until 6:30-7:00 a.m., when they would retire until 
the following evening. During the summer, they retired later — 
between 7:30 and 9:00 a.m., usually to the cool basement of the 
second house, or they would move to this basement from the 
flaphouse sometime during the day as the ambient temperature 
rose up to 30°C (86°F). The later returns to shelter in the morn- 
ing always followed a i-iVi hr period hunting squirrels in the park, 
an activity which was not evident earlier in the study. A kill of 
squinels was never observed. Activity was greatest then from 
around midnight to early morning, during which time the ambient 
temperature averaged some 7° less than during the day. A lower 
temperature in the evening and early hours of the morning would 
be anticipated but the buildings and pavements of this humid city 
give off much absorbed day heat during the night. 

The night and early morning activity was interspersed with 
rest periods of varying duration (see Figure 2); the trio never re- 
turned to the cover of its houses during this time (even during 
heavy rain), preferring to sleep out in the open, on lawns or 
porches of occupied houses. When active, they would systemati- 
cally forage for food in the three alleys and in backyards which 
opened onto these alleys (see Figure 3). Interactions with other 
dogs occurred during these times and also in the park, and these 
will be described later. 

Interestingly, the head counts of free-roaming dogs which 
gave a good index of the activity of other dogs in the neighborhood 
did not follow the pattern of the trio during the day and early 
evening (see Figure 4). Whereas the trio were under cover during 
the day, free-roaming dogs showed two peaks of activity — 
between 9:00 and 10:00 a.m. and around 7:00 p.m. The dramatic 
decline in head counts between 6:00 and 9:00 a.m. corresponds 


THE dog: its domestication and behavior 


Figure 4. Activity index of free-roaming dogs in study area 
{number counted over a Vi-'hr period). The nctivity of the feral trio 
is superimposed for comparison. The latter show no late morning 
(8:oO'9:oo o.m.) or early evening (7:00-9:00 p.m.) och'oify peflfcs 
and are most active during the early hours of the morning. Data 
averaged from 90 hrs obseruoHons. 

with many of the free-roaming dogs returning home, presumably 
to be fed when their owners arise. The evening peak also correlates 
with human activity; the streets are full of diildren playing and 
adults conversing on their porch steps. The feral trio was never 
seen out at this time, and it may be concluded that they were 
avoiding human contact. Most dogs avoided the hottest time of the 
day between 2:00 and 4:00 p.m.; free-roaming dogs, like the feral 
trio, were most active during the early hours of the morning, 
shortly before sunrise (Figure 2), 

Behavior and Ecology of an Urban Feral Dog 



The trio's main area was located within a low income, primarily 
abandoned, residential area of about four city streets of 427.5 m 
(1402.5 ft) long in each direction and 33-5 ^ representing an 

available surface area of about 5.7 ha (hectares) (14.2 acres) exclu- 
sive of inner buildings. In the mornings, they often used much of 
an adjacent 55.3 -ha (136.6 acres) park (477.6 m x 1156.7 m) or a total 
home range of 61.0 ha (150.7 acres). This area is considerably larger 
than the area used by a group of two feral dogs observed in 
more, Maryland (Beck, 1973) possibly indicating a less favorable 
habitat, i.e., food availability. Home range for many animals is 
probably influenced by food availability (McNab, 1963)*^^^ oxes, 
Vulpes fulva, were observed to have smaller ranges in ° 

greater ecological diversity than those in suboptimal habitat (Abies, 
1969). Feral dogs in rural Alabama have home ranges grea er an 
1,000 ha (Scott and Causey, 1973) possibly less available 

food. It would be interesting to investigate the hypo esis 
urban populations have smaller home ranges than t eir , 

counterparts, which appears to be the case even 
Human activity and construction may provide or a ,’S , 

of food and cover resources and artifacts in t e 
might be used by animals on occasion-all of which would faali 

"" rh^h^trio kept to a fairly regular H- 

tended to stay within a predictable home ran^ ^hid never been 

they twice went into two separate areas ‘ jniolcrant 

seen to go before. In one of these, resident ^ogs 

toward the trio and actually chased them ranee- these 

contrast to the dogs that lived within the temis with the 

dogs being more tolerant, some even o hv huncer to 

go into these new areas since they had r T ge 

fact, forage for food in these new are ■ jub- 

extending their effective home r^g ^ 

sequently return to these areas. The t ° noint after a night 

cursion was 1.7 km (1.06 mi) measured point to point 

of movement across their range. 

52 - 

THE dog: rrs domestication and behavior 


The frequencies of marking in various contexts are shown in Table I. 
Both males marked more than twice as often as the female (F), who 
never, in fact, marked in the presence of a strange dog. Marking in 
the alleys of the home range and in the park were at a similar 
frequency for X and F, but Y showed a greater frequency of mark- 
ing in the park than in the alleys. The role of the marker may 
change with a change in locale, X being the most frequent marker of 
the home site area (alleys), while both males mark almost equally 
in the park. Y marked more frequently than X in the presence of a 
strange dog and was the most aggressive of the trio toward strang- 
ers. The low incidence of scraping after marking in X may be due 
to his hip injury; F was never seen to scrape. Marking over, that is 
marking where another conspecific has just marked, may be a very 
significant social phenomenon in the dog since it was one of the 
most consistent findings in our study. Of the 36 times that F uri- 
nated, one or occasionally both males were seen to mark over her 
mark 30 times (see Table I). Twice, F marked over X. One occasion 
served to demonstrate the intentionality behind this behavior: 

4:15 a.m. X crosses the road while F pauses to sniff the 

sidewalk. F urinates, then runs to join X but X sees 
her and comes back to mark over. He then crosses 
the road again and continues on his way with F and 
Y following. 

X marked over F three times as often as Y; this may indicate a 
closer allegiance with the female F. Interestingly, X marked three 
times over Y after Y had marked over F. Y was only seen to do this 
once (marking over X's mark over F). What stimuli initiated mark- 
ing in the first place were not determined. Often a horizontal sur- 
face was marked (grass clumps, lawn, edge of pavement), but 
more often a vertical object was marked (wall, comer of a wall, 
tree, fire hydrant, lamp post or trash can). Marking was particu- 
larly evident when the trio entered the park early in the morning. 


The observed frequency of which individual led the trio when mov- 
ing within the home range after resting or eating is shown in Table 

Behavior and Ecology of an Urban Feral Dog 


*ms. m.uVs and ^cr.ipvs 


THE dog: its domestication and behavior 

Table II. 


After resting, eating, and 


ranging in park 

Leads chase in park 










II. The frequency of leading while ranging in the park and while 
chasing squirrels is also included. Clearly, in the home range, the 
female (F), was the usual leader. X usually followed F, and Y would 
then often follow the pair, possibly a magnet effect (see later). Male 
X tended to lead to the lake in the park where the trio would drink 
and swim and was also the one to lead the group back from the 
park (see Figure 5). Male Y tended to lead active chases in the park. 

Leadership entailed a number of subtle overt signals, espe- 
cially eye contact. For example, F or Y would wait for X to catch up, 
often sitting and looking back at him. As soon as they looked back, 
he would speed up. After resting, F would stand up, walk off a few 
paces and then turn and look back at X and Y. This looking back 
stimulated them to follow. F would then run or trot a few more 
paces and look back. If they were not yet following, she would 
stop, look back and then give an exaggerated head turn in the 
direction she was heading. The following anecdotes from our field 
notes will further clarify this subtle communication: 

2:50 a.m. Trio sleeping on porch. F gets up, gives a yelp bark 
and goes down steps onto sidewalk with Y. X sleeps 
on. F returns 5 min later and gives another yelp bark 
and a tail wag toward X. X gets up and follows her. 

F face-rubs and tail-wags with X. 

3:55 a.m. Trio sleeping. F stands up, looks at Y. Y im- 
mediately sits up. F gets off paHo and goes onto 
sidewalk and looks back at X and Y. She then sets 
off down the road. Y stands up. F stops and looks 
back at Y. Y now follows her. X still sleeps. Y looks 
back at X, then follows F. After 5 min, Y and F re- 

Behavior and Ecology of an Urban Feral Dog 


turn to patio. F tail-wags at X who is still sleeping. Y 
sits close by and tail-wags. X sits up. Y moves off. F 
waits by X. Y returns to porch and tail-wags at F. F 
goes onto sidewalk and looks back at X. X stands 
up, marks twice and Y marks and scrapes. Y crosses 
road and looks back at F. F (in middle of the road) 
looks back at X, who joins her "at last." She gives a 
tail-wag, face-bump and exaggerated head turn to X 
and then leads him across the road to join up with 
Y. With F in the lead, Y and X follow her to forage. 

The following interacHon illustrates further the dynamics of 
communication between two members of the trio. X is wit a resi 
dent free-roaming female who is in heat. 

8:30 a.m. F moves off and looks back at X. X looks at 

lows her for a few paces, then stops and looks back 
at the estrous female. He then returns 
female. F moves off again a ® * F 

and looks back at X. X looks at F and then follows F 

back to the flaphouse. 

The magnet effect of the trio keeping together is exemplified 
by these two observations: 

4:30 a.m. F crosses the main highway but X -d Y stay on the 
sidewalk and do not follow; F returns to them 
all three go off in a different direction. 

7:15 a.m. Y crosses the main and d^not fol- 

park; X and F stay on the other two. 

low. Y looks back and then rejoins the other tw 

Further notations on on^hunHng acHvity in'^the 

sented subsequently in the observatio 


eve contact (looking 

In this category, overt and waiting for a con- 

at), and covert communication of to i„.dership). Only overt 

specific, are not included (see section o 

Figure 5. Trio behavior in the p 
bathing and drinking in lake, (d) i 
one spatial pattern while looking 
scraps, and (g)F and Y wailing fot 
before leflviwp park. 


sodal behaviors associated vv'ith ^ considered. Among 

aggression, and social investigation wiU ® recorded 

members of the trio, a total of only i6 in .chance of this un- 
tliroughout the entire study. The possi ® ^ discussed sub- 
expectedly low frequency of overt be 

sequently. observed behveen X, F, 

No displays of submission were e erovvied at X and Y, 

and Y. On two occasions during feeding, interactions, 

respectively, and both withdrew. Of the 14 included bnef 

all were friendly and of extremely short dura nose- 

taU-w;,a.Hr,cr face-bumping or ruboing. 

were friendly and of extremely sno tnhbine 

1-wagging, play-bow, face-bumping or 


THE dog: its domestication and behavior 

DUshine toward the mouth of a companion. One bnef (5 sec) play- 
*ase 4s recorded in the park between F and ^ 

summarized in Table 111. X initiated no mterachons himself engag- 
ine in one redprocal face-rub and tail-wag with Y when the latter 
rejoined the trio after a brief absence. Possibly an indicator of soaal 
preferences, the female F initiated more interactions toward X than 
toward Y, while Y interacted almost equally with X and t. 

Interactions with other dogs, some identified as free-roammg 
residents that shared the same home range as the trio and 
nonresident free-roaming and feral dogs were as follows: Ot 33 
recorded encounters, sb< were designated neutral where the 
stranger approached the trio or passed by and was ignored. Eight 
interactions were judged as friendly, since reciprocal tail-waging 
and, more rarely, play acHons were observed (see Table IV). Nine- 
teen other interactions were aggressive or offensive. On one of 
these occasions, a dog crossing into the park was intimidated by 
the mere sight of the trio and ran off (none of the trio even looked 
at the dog), and it was hit by a car. More often the strange dog would 
be intimidated by Y and would run off. On eight of the aggressive 
occasions, Y was the main instigator of intimidation toward strangers 
(see Table IV), On one occasion F supported Y in chasing a stranger. 

Table HI. 













F F F F F* (5) 





F F F F (4) 


F F F (3) 



•RF, r«?ciprt>cal friendly interactions. 
'A, agonistic interactions. 

*F, friendly Interactions. 

Table IV. 



Y barks at SD 6 and chases; 

F supports Y, barks and chases. 

Y then urinates. 

SD approaches and stands still. Y 
alerts and looks; SD ? runs off. 

F barks at SD. Y chases SD and 
then returns and tail-wags to 


Mange-covered SD 6 challenged 
by F. No submission, briefly 
follows trio. Ignored by X and 


*SD <5 approaches, chased by Y. 

Y approaches SD 6 who runs off; 

Y marks. 

SD 9 approaches submissively; 
X, supported by F, chases her 

Y chases approaching SD ?, then 

SD ? sees trio, retreats though no 
obvious threat. Y marks. 

•SD 6 approaches; X tail up, side 
on threat. Y play-bows to SD, 
then rushes and bites scruff. 

SD runs off. Y play-bows to X, 
then marks. 


Y approaches resident 6, recip- 
rocal tail-wag and genital 

Y approaches resident d, genital 
sniffing, then Y marks. 

•Y approaches SD 7, investi- 
gates, then gives play bow and 
F prances. 

Y approaches with tail-wagging 
and investigates SD ?. F ap- 
proaches, X follows and SD 
runs off. Y marks. 

•F meets 2 6 SDs; social investi- 
gation and reciprocal tail-wag 
but F intimidated until Y joins 
her and greets the 2 ds. X 

SD 9 approaches, gives low tail- 
wag to Y, who reciprocates 
with high tail-wag. SD 9 also 
tail-wags to F and X. Trio leave. 

•Trio meet SD d, SD 9 and SD d 
pup; reciprocal greeting and 
social investigation. SD 6 pup 
joins trio briefly. 

■Symbols: ?, indicates sex of SD not determined; •, occurred in park. Ail other 
observations in alleys. 


THE dog; rrs domestication and behavior 

pushing towatd the mouth of a companion. One brief (5 sec) play- 
chase was recorded in the park between F and Y. These data are 
summarized in Table III. X initiated no interactions himself, engag- 
ing in one reciprocal face-rub and tail-wag with Y when the latter 
rejoined the trio after a brief absence. Possibly an indicator of social 
preferences, the female F initiated more interactions toward X than 
toward Y, while Y interacted almost equally with X and F. 

Interactions with other dogs, some identified as free-roaming 
residents that shared the same home range as the trio and others as 
nonresident free-roaming and feral dogs were as follows; Of 33 
recorded encounters, six were designated neutral where the 
stranger approached the trio or passed by and was ignored. Eight 
interactions were judged as friendly, since reciprocal tail-wagging 
and, more rarely, play actions were observed (see Table IV). Nine- 
teen other interactions were aggressive or offensive. On one of 
these occasions, a dog crossing into the park was intimidated by 
the mere sight of the trio and ran off (none of the trio even looked 
at the dog), and it was hit by a car. More often the strange dog would 
be intimidated by Y and would run off. On eight of the aggressive 
occasions, Y was the main instigator of intimidation toward strangers 
(seeTable IV). On one occasionF supported Y in chasing a stranger. 

Table III. 










1 RF* 


F F F F FM5) 





FFFF(4) I 

F F F (3) 



*RF, reciprocal friendly interactions. 
M. agonistic interactions. 

'F, friendly interactions. 

Behavior arid Ecology of an Urban Feral Dog 


fined resident dogs and the trio, while foraging in the back alleys of 

On three occasions the trio howled to passing police car sirens. 
They avoided people, especially children, Y having the greatest 
flight distance. In the park, people were often ignored. Relation- 
ships with cats were consistent. All three observed encounters re- 
sulted in chasing, and on one occasion a cat was almost caught by 
F. One rat kill was observed in a back alley; this was the only live 
prey the trio was ever seen to secure. 


The frequencies that any individual was not in the trio for any 
period of time greater than 3 min were as follows. F broke the trio 
twice for 5 min, once with another nonresident male dog and once 
to forage alone. X was not with the other two dogs on only two 
occasions, once when he returned 5 min early from the park and 
once when he refused to get up and continued to sleep for 5 min 
before F and Y got him to follow them. Y was the most often away, 
F and X being seen together in the absence of Y a total of 15 times, 
indicating that Y may have had a lesser tie to the group. He would 
often sleep alone in one of the houses. Since we do not know the 
origins and earlier relationships of these dogs, no further conclu- 
sions can be drawn. Usually no greeting or overt interaction was 
evident when Y rejoined the other two dogs. 


Shortly after the initiation of the study, the trio, instead of retiring 
for the day around 6:30 a.m. would go to a park adjacent to their 
home site for 1-2 hr. (Since they later stopped going to this park, 
we may conclude that this was a summer schedule activity.) 
In the park, the trio would scavenge profitably for food under 
park benches and picnic tables, but most of the time in the park was 
spent chasing squirrels. On entering the park and marking, they 
would trot across open space and then break into a ranging run 
beneath the trees. If any squirrels were seen on the ground, they 



Both Y and X were seen supporting F in intimidating an approach- 
ing stranger. 

More rarely, a strange dog would join the trio for varying 
periods. One resident free-roaming dog, a male, was seen foraging 
with the trio early in the morning on three occasions. Another 
morning, a small male pup played with F in the park after meeting 
the trio earlier in a "morning greeting" (described below) and also 
briefly joined the trio to hunt squirrels in the park. The most in- 
triguing temporary union of a stranger with the trio occurred one 
morning. A male dog, about the same size as F, stayed with the trio 
from 4:42 a.m.-7;40 a.m. while they foraged in the alleys. When 
the trio returned to one of its houses, he remained outsi^._The 
field notes summarize what followed: 

7:30 a.m. F comes to the front door of the abandoned house 
(Y and X have retired upstairs). The stranger, a 
brown male (Br), looks up at F, tail high and wag- 
ging, and marks the porch. F comes down the steps 
and leads Br to the flaphouse. He follows her up 
the steps. Meanwhile X comes out of the back door 
of the first house and trails the pair. X and F go into 
the flaphouse while Br waits on the steps. 

His approach/withdrawal behavior in front of the door indicates his 
ambivalence about entering the unfamiliar house. After waiting 2 
min, he leaves. This dog was never seen again by the observers. 

Toward the end of the study, a young female dog joined the 
trio for an estimated 6 days; it was subordinate to F but was ac- 
cepted by her. 

The trio was seen once involved in one of three observed 
morning greeting ceremonies where several dogs come together 
and engage in reciprocal social investigation and greeting (see 

The trio was on friendly terms with two separate dogs who 
were usually tethered in their backyards. During the early hours, 
the trio would enter these dogs' backyards, were usually greeted, 
and would eat out of the dogs' food bowls and forage in the gar- 
bage cans in the yards. They would often rest or rendezvous after a 
brief separation in these yards and use one as a regular crossing 
betrvoen streets. Tail-wagging was often noted between other con- 

Behavior and Ecology of an Urban Feral Dog 


The dogs expended considerable energy on these mornings in the 
park. The adaptive significance and bioenergetics of this hunting 
behavior are questionable since out of a total of 61 chases (see Table 
V) no squirrel was ever caught. This activity may be reinforcing 
itself, i.e., like play. 


The occurrence of dogs seen alone and in groups of two or more in 
the area of study and in adjacent regions is summarized in Table 
VI. Most dogs were seen singly, although pairs of dogs were com- 
mon. It was not possible to sex all pairs observed, but where it was 
possible, either two males or a male and female were together. No 
female pairs were identified. SN trios of dogs were seen, two of 

Table VI. 


Number of dogs together 

3 2 , 3 4 5 6 7 


moving or foraging 161 30 6 

With $ in heat _ ~ 4 groups 

of 3 <Js 

9 with pup(s) — with — 

1 pup 

Pups alone 

without mother — 1 ^ 

With people 14 — 

“Greeting" group — — 

foraging in 
same vicinity) 

— 12 4 

9 with — — — 

3 pups (X 2) 

Total count 

175 64 



10 18 35 


THE dog: its domestication and behavior 

would immediately give chase. The trio would systematically work 
over different areas of the park where there were stands of trees. 
Once, and often twice each morning, they would drink and bathe in 
a large lake in the center of the park for 2-3 min. Bouts of chasing 
and ranging were interspersed with resting periods, when the trio 
would lie or sit in three patterns of head orientation (see Figure 5). 
These patterns optimized the chances of spotting a squirrel and as 
soon as one dog alerted and oriented (and occasionally tail- 
wagged), so would the other two. If it then gave chase, the other 
two would follow immediately, correcting their orientation when 
they too saw the prey. This later orientation often resulted in one 
dog bumping into a companion or momentarily running in the 
wrong direction. Also, while in a ranging run if one dog suddenly 
ran to one side upon seeing a squirrel, the others would follow at 
once and then look. If, for example, the center dog in Figure 5e 
suddenly alerted forward, the dogs on each side would alert in the 
same direction. If the dog on the far right in Figure ye alerted in a 
forward direction and to its right, the other two dogs would turn 
around quickly and orient to their left. 

Chases were usually terminated by the dogs jumping up at the 
tree in which the prey had sought refuge (see Figure yd). F and, 
less often, Y would jump up against the tree, and barking and 
taU-wagging were frequently noted. On two occasions, squirrels 
were seen to jump out of the trees up which they had been chased, 
while the dogs were barking and jumping up at the base of the tree. 

Table V. 




Time of onset 

Number of chasesIHme . 

June 8 


5;15 a.m. 

6 chases/190 min 

June 11 


5:35 a.m. 

30 chases/170 min 

June 13 



5:33 a.m. 

10 chases/180 min 

June 15 


5:15 a.m. 

10 chases/225 min 

July 9 


5-35 a.m. 

5 chases/120 min. 

Behavior and Ecology of an Urban Feral Dog 



Against the background of Beck's (1971, 1973) studies of urban 
dogs, the present study focuses more specifically on the social 
ecology of a pack, or social unit, of three animals. Permanence of 
such a social unit may be rare in urban dogs, but this conclusion 
awaits further study. The distribution and abundance of food (i.e., 
wide dispersal, but in small concentrations) would favor solitary 
scavenging, and all other feral dogs observed during this study were 
seen singly and more rarely in pairs.* Groups of three or more were 
usually temporary packs of males following a bitch in heat. A per- 
manent pack in the urban environment would also be conspicuous 
and more liable to human predation (the local dog catcher chases 
groups more than individuals). 

In relation to the diurnal activity of other dogs, the feral trio 
remained undercover during the major part of the day. This may 
have been to avoid the heat of the day or human interactions, or 
both. They clearly avoided close proximity with people, while the 
activity of nonferal dogs closely coincided with human activity, 
i.e., a morning peak around 8:00 a.m. (when many are presumably 
let out of the house) and a peak in the early evening when dogs, 
people, and children would be out in the streets. Nonferal dogs 
were least active during the afternoons, the hottest time of the day, 
and, like the feral trio, were most active during the early hours of 
the morning. 

In contrast to the regular morning visits of the trio to the park 
to scavenge for food and to chase squirrels, other dogs were only 
occasionally seen there and without any regularity in their visits. 
The amount of time and energy the trio spent in ranging over the 
park and chasing squirrels, which they were never seen to catch, 
was remarkable. Such unreinforced activity may be rewarding in 
its own right and could be interpreted as play. 

The interacrions between the three dogs were surprising, since 
much more overt communication and social interaction were an- 
ticipated. There was little "redundancy" however, and much 

•Feral and free-roaming dogs observed in Mexico Cily and Madras n ere seen forag- 
ing singly and only occasionally in pairs (M W Fox) 


THE dog: its domestication and behavior 

which were foraging, two playing, and two traveling. Three early 
morning greeting groups of respectively 5, 6, and 7 individuals 
were seen. These groupings were of extremely short duraHon (1-3 
min). Groupings of longer duration were focused around a female 
in heat: four groups of 3 males and 1 female, one group with 5 
males and 1 female, two groups with 6 males and 1 female and 
three groups with 7 males around 1 female. A major stimulus for 
temporary pack formation in the urban dog is clearly the presence 
of an estrous female (see Figure 6). 

Figure 6. Free-warning house dogs forming a temporary pack 
awund an esiwus bitch (a), creating a traffic hazard crossing 
highieay (h>, and attempting to reach the bitch who is seeking ref- 
uge under an automolrile (d). The resident was unable to leave the 
house for fear of being attacked as the temporary pack rests on her 
front steps (c). 

Behavior and Ecology of an Urban Feral Dog 


disease problems, both pre- and postnatally, would reduce the 
chances of any offspring surviving up to weaning age. Toward the 
end of this study, F was reportedly in heat (September, 1973) ac- 
cording to one local resident, and further observations confirmed 
that she was pregnant (or pseudopregnant). If any pups were 
bom, they could not have survived long since we were unable to 
find them although the trio was still active in the area through 
January. While Nesbitt (1975) has shown that there is some natural 
selection in feral rural dogs for a particular body size/phenotype, it 
is unlikely that natural selection could operate in feral urban dogs 
because of the high turnover rate of the population and low chance 
of survival for any offspring. 


A group of three feral dogs (two males, one female) living in vacant 
buildings in St. Louis, Missouri was studied. They avoided close 
proximity with people and were active earlier and later in the day 
than the people and loose pets in the area. They found food while 
scavenging throu^ human trash. The group'^s activities were usu- 
ally initiated by the female of the group though otherwise there 
was no clear linear hierarchy and few ritualized displays of domi- 
nance or greeting. Specific roles within the group were observable. 
Though the female appeared to be pregnant during the study, 
puppies were never noted. 



communication was overt, involving body orientation and eye con- 
tact. It must be concluded that each member of the social unit was 
fully aware of what the other dogs were doing and were intending 
to do much of the time, i.e., a metacommunicative system and 
context-related set of expectations were operating. In addition, 
since there was no clear linear dominance hierarchy, there were 
few ritualized displays of dominance and submission and no greet- 
ing rituals to the alpha individual (as exemplified by the wolf pack, 
[Fox, 1971b]). Leadership, i.e., choice of direction of movement, 
was usually made by the female, who at such times could be desig- 
nated leader. On two occasions (while feeding) she asserted domi- 
nance over the others by staring and growling. The response was 
nonsubmissive avoidance. Competitive behavior was never seen 
on other occasions. 

In relation to context, therefore, individual differences were 
evident, and in different contexts the female was the leader or was 
dominant. If behavior differs between individual members of a 
social group in the same context, then the possibility of context- 
related roles in relation to the social ecology of the group must be 
considered. Two of the dogs of this social group appeared to have 
different roles which were apparent at different times in certain 
contexts. While the female was most often identifiable as the 
leader or decision-maker, the male (Y) was the most aggressive 
toward strange dogs and might be designated as the guard of the 
unit, A specific role for the other male (X) was not so easily as- 
signed. There was no evidence of dominance over, or subordina- 
tion to, the other male, and X marked (the home range) 2.6 times as- 
frequently as Y (except in the park) and marked three times as 
much as Y over F after she had urinated. This latter observation 
may indicate a closer bond behveen X and F than between F and Y, 
an interpretation supported further by the fact that Y left the social 
unit more often than either of the other dogs. Also the female (F) 
initiated more social interactions with X than with Y, while Y in- 
teracted at almost equal frequencies with X and F. There was no 
ewdence that the marks were cither used or respected as territorial 
boundaries in this feral trio. 

In spile of these feral dogs' remarkable abilities to adapt to the 
urban environment, it is unlikely that they could succeed in raising 
a litter of pups under such conditions. Nutritional, parasite, and 


Vocalizations in Wild 
Canids and Possible 
Effects of 


In order to make an inventory of the various sounds emitted by 
canids, the vocalizations from several different species of Canidae 
reported in this study were recorded, and selected sounds were 
analyzed on a sound spectrograph. From such an inventory, m- 
terspecies comparisons of vocalizations and of the vanous contexts 
in which they occur could lead to a closer understanding of 
taxonomic interrelationships. It might also throw I^ht on the on- 
gin(s) of the domesticated dog Cams fmmlmns which is, to dale, an 

^™^“e study of canid vocaUzations is also of significance for other 

reasons. Firsh an understanding of *”''ntcT 

mals is a necessary part of understanding their total communica- 
tion system (Fox and Cohen, 1977). foj 'he 
enhance visual and olfactory displays but in 

as a substitute for these displays, as f domic 

cover, or at night. Second, the canid family is 

in some respects. Its members come from a " 'do v. ncU) o sr^al 
systems (Fox, 1975) ranging from the greganous (eg., ivohcs. 

Vocalizations in Wild Canids 


Table I. continued 









































































•Most sounds are not mixed, but some of the sounds may be mixed simultaneously 
or successively, e,g., whine-growl, bark-howl, yelp-bark. 

‘F, red, arctic, and grey fox; D, dog; W, wolf; C coyote; N, neonates of these species. 
•Also "contentment grunts" of contact in neonate W, C, and D. 

•“May serve as warning to others. 

3 wolves {Canis lupus) from birth to 2 years 

2 red foxes (Viilpes vulpes) from birth to lo weeks 

4 red foxes from 2 weeks to 10 weeks 
4 red foxes from 2 weeks to 3 weeks 

2 grey foxes (Urocyon cineraoargentcus) from birth lo 10 weeks 
2 grey foxes from 8 weeks to 2 years 
8 Chihuahuas from birth to 6 months 


4 coyotes (Cams latrans) from birth to 3 years 
4 F. coyote X beagle hybrids from birth to 3 years 
2 ArcHc foxes (Alopex lagopus) from 8 rveeks vmrs 

2 Asiatic golden jackals (C. aurens) from i week to - > cars 


THE dog: its domestication and behavior 

Table I. 


Social Context 





































Care- or con- 




N of WCD; C 



Distress (pain) 




N of WCD; D 


(lone calls) 



Group vocali- 




rela«vely nonsocial (e.g., foxes). Com- 
fFnif "'m greatly between these two main groups 

box, i9^b), and comparative studies may add to our knowledge of 

knowSlHoo ^ evoIuHon of canids. This. 

icement^fT^J essential to the preservation and man- 

agement of endangered species. 

Materials and 

Over a penod of 7 years, recordings of vocalizations were made of 
the following speaes at various ages (the animals were all hand- 
raised m captuTly): 

Vocalizations in Wild Canids 


from more complex mixed sounds, which are described shortly. It 
should also be emphasized that under the categories of whines and 
coos, for example, there are clear differences between and within 
species in the pitch, duration, and spectrographic structure of such 
sounds. The focus of this study, however, is not to look at such 
species and individual differences within sound types but rather to 
make an overall survey of the occurrence of these basic sound 
types across species to provide a basis for evaluating the possible 
effects of domestication on canid vocalizations.* 

The cross-species survey clearly reveals the distinction be- 
tween vulpine (foxlike) and canine (dog/wolf-like) species, the 
former showing a high incidence of coo-calls and guttural clicks 
(absent in the latter), a high frequency of screams, and an absence 
of group vocalizations. The yip sound type was exclusive to 
coyotes and golden jackals, and a high incidence of barks in many 
different contexts was characteristic of the domestic dog. No var- 
iations in occurrence of sound types in individuals of the same 
species were ever recorded in different contexts, i.e., sound type 
and context specificity was evident for each species studied. 

In addition to these vocal sound types, aU species commurii- 
cate to some extent by means of mechanical or unvoiced sounds 
such as the tooth-snapping heard in wolves, coyotes, and dogs, 
and panting, a play-soliciting signal of dogs and foxes (see page 
135). Because these mechanical sounds are of relaHvely low volume 
and do not carry very far, they are reserved for close contact situa- 
tions and are often heard during agonistic encounters. 


Some evidence is available at this point to warrant preliminary 
cross-species comparisons (see Figures 1 an z). 

t differences, which is in itself 

"This is not to underrate the significance o ‘ ^lear indi^Tdual dif- 

an important and much needed area as for example, wolves engaged in 

ferences became evident during the s j,fferenl sexes emitting the vime c«x> 
group howling and in red and grey oxes duration Such vanations could 

rail in nifrh. form, intensity, ^ state and intentions 

call varying widely in pilch, fhe emotion-i 

permit even more information excha g 
per se that are discussed in this chapter. 

7 ^ 

the dog: its domestication and behavior 

Recordings were made in nine different social contexts listed in 
Table I. In addition, recordings were also made of various zoo 
animals including Dingo {Canis exfamiliaris dingo). New Guinea 
singing dog (Canis exfamiliaris hallstromi), maned wolf (Chrysocyon 
brachyitrus), culpeo (Dusicyon culpaeus), wolf (Canis lupus), coyote 
(Canis latrans), bush dog (Speolhos venaticus), and Cape hunting dog 
(Lycaan pictus). 

All recordings were made on a Sony EM-2 field recorder at 7 
in. per second. South analysis was then performed with a Kay 
Sona-graph 6061A, with high shape (HS) and narrow band set- 

Later references to short, long, or extended sounds refer to 
arbitrary classes of sound duration as follows; short, 0-0.9 loTig, 
1.0-2.4 sec, extended, 2.4+ sec. 



Twelve basic canid sound types were identified in this study includ- 
ing whines (and longer softer whimpers), short yelps, yips, 
screams, barks, coughs, growls, coos, howls (or yowls), mews, 
grunts, and guttural clicks. Variation within these categories may 
occur at both the individual and interspecies levels, and sounds 
may vary along the dimensions of duration, frequency, intensity, 
cycle (rhythmicity), and context. 

Not all of these basic sound types arc included in the vocal 
repertoires of every canid species, and the same sound may be 
used by different species in very different contexts. Foxes, for 
example, are the only canids known to emit a pure scream in greet- 
ing conspecifics, and domestic dogs will bark in many situations 
(c.g., threat, play-solicit, contact-seeking) while foxes bark only in 
threat. The presence or absence of these various sounds in dif- 
ferent canid species is shown inTablel together with the context(s) 
in which each sound was recorded. Further descriptions of some of 
these basic sound types may be found in Tembrock (1968, i960), 
Bleichcr (1963), Joslin (1966) and Thebergc and Falls (1967). 

The basic sound types listed in Table 1 are to be differentiated 

Figure 2. Mixed sounds. Successive: (A) bark-^growl of a 4- 
week-old male Chihuahua: (B) pure coo and coo^scream of a 
i^-day old female red fox; (C) yelp-rgroiol-rbark-^grou>l of a 
lo-day-old male Irish setter X Doberman pinscher. Stmultane 
ous: (D) bark-howls of a i-year-old female wolf: (E) growl- 
scream of Culpeo: (F) growl-scream of a y-month-old female 
Arctic fox. 

cated a fundamental and PDF of 1500-3400 Hz. ^hirang is most 
often a cyclic (i.e., rhythmic) vocalization given m ^stress, with 
the exception of the undulaHng whine which is noncyclic. 

"'"'^hese sounds, as shown by Bleicher (^963). ^lop in 
in combination with the whine ^vhine ^discussed 

successively combined with a grow , ' in other adult 

later). This particular sound type ^ ^ ■ familiaris. For 

canids and may be a species-charactenstic 01 cai. 1 hortened, 

the purpose of this study, the yelp d piercing variant, 

contracted form of the whine; a high jackals. 

the yip, being an ®°"^/g“[ext in the fox is the scream. 

The analogy of the yelp in the same c 



Figure 1. (A) Whines of a , -day-old male Chihuahua. (B) 
Screams of a 6 -day-old male Chihuahua. (C) Barks of an adult 
fmale dingo. (D) Crawls of an adult male wolf. (E) Coos ofan- 
ioy-fd female red fox. (E) Excerpt from a howl ofan aduti female 
wolf (C) Mrros of e y-week-old male Chihuahua. (H) Grunts of 
an 8 -day-old male Irish setter X Doberman pinscher hybrid. 

ratiol^ I i !f short du- 

Hmes “bservaKon) will some- 

hmes extend this sound for several seconds, however orodudne 

Tound whine (Crisler, '1958) Thif 

cadw altemaM W w ‘ongue within the vocal 

ravity alternately blocking and opening air passages (Crisler, 1958). 

the whiner'^f <* 0 "''nant frequency (PDF) found in 

the whines of adult wolves were both about 1570 Hz TTie same 

figures apply to the undulating whine nz. me same 

whill^he PnP™""'"' u ^ ^"Ses from 400-1570 Hz, 

uhile the PDF is usually from 2000-3000 Hz. Recordings made of 

developing Insh setter x Doberman pinscher hybrid puppies indi- 

Vocalizations in Wild Canids 


but not analyzed, in all canids. It may serve as a warning to off- 
spring and others in agonistic contexts. 


All recorded howls of wolves and coyotes were of long to ex- 
tended duration. The fundamental for both species was between 
400-2000 Hz and the PDF from 1200-2900 Hz. 


Preliminary evidence indicates, that newborn to 5-week-oId 
red and grey foxes tend to repeat their neonatal mews more often 
than dogs of the same age group. Foxes maintain this sound as part 
of their vocal repertoires throughout life, while it is only heard in 
neonates of all other canids studied. 

The fundamental of the grunts of wolves and dogs ranged 
from 85-200 Hz when detectable. The sounds are heard in neon- 
ates of these two species and the coyote but were not recorded in 

This sound is heard only in foxes. One fom is trill 1 ^^ 
the other is more of a cackle. Differentiation e 
on the basis of spectrographic evidence is difficult, and it is not yet 
clear which stimuli elicit each form of the coo. 


The above sound types may be mixed 

superimposition of two vocal sounds o y , ; n /-pp Fieure 

tw"o or m"ore types of sounds (vocal andf^rmech^ 

2). A combination of these two mixe follow a pure 

a mixed sound, for example, ""'S correlafes ivell with the 

sound. The phenomenon of sound m g expressions 

superimposiKon of body 'artgoage pos eliciting 

(Fox, 1971b). A wolf faced with a situahon s 

•Tliis sound type is to be distinguished from the gntuj end gntn.s of u, nr dung 

canid, or of one in intense pain as dunng pa 


THE dog: its domestication and behavior 


The screams of red foxes tend to be of longer duration and 
occur in a greater variety of contexts than those of other canids. 
The gray foxes recorded emitted screams which were generally 
shorter than those of the red foxes but were repeated more often. It 
is thus possible that the total signal value of the scream for these 
two species is about equal. The fundamental for most foxes studied 
(including the Arctic fox) ranged from 1200-2000 Hz. The PDF was 
between 2000-5000 Hz. Chihuahua recordings indicate a funda- 
mental of 1200-2000 Hz and a PDF of 2000-3200 Hz. Recordings of 
Irish setter X Doberman pinschers show fundamental and PDF val- 
ues between 1800-2700 Hz. Preliminary data on the screams of 
coyotes indicate a fundamental of about 2400 Hz and a PDF of 
about 2700 Hz. 

The scream is noncyclic in red foxes and repeated, but not 
cyclically, in gray foxes. Chihuahua puppies given painful skin 
stimulation screamed noncyclically. Those placed on a cold sur- 
face, however, emitted cyclic screams. 


Barks of all species recorded were of very short duration (i.e., 
0.5 sec). All principal frequencies (fundamental and PDF) lie in the 
lower register between 0-2000 Hz. The main differences between 
the barks of various canid species concern cyclicity. The domestic 
dog will often bark cyclically in a singsong manner, one bark fol- 
lowing another until a train of barks results. This is commonly 
heard during territorial defense and care or contact solicitation. 
Foxes bark noncylically, while our data indicate that wolves may 
bark either cyclically or noncyclically. Further investigation is 
needed to distinguish the different stimulus situations that elicit 
these two barking forms in wolves. 


Growls may vary in duration from short to extended, depend- 
ing on the situation and intensity of the social encounter. The 
growls of all species are noncyclic. While foxes growl only in threat 
and defense, wolves and some dogs growl while greeting one 
another possibly reaffirming their dominance relationships. 
Wolves, dogs, and especially coyotes may often growl during 
group vocalizations. A muffled growl-bark or cough was recorded. 

Table III. 


Vocalizations in Wild Canids 


I I I 

u 1 I 

.. I I 



I I 
I I 




I I I 

O Q 

I I I 



I I 
I I 

I I 

I I 

i d C 

.ibbrcvl.Mcd form~lhc yelp and yip. 

*D. dt^meMte doR, W. woU: C. coyole; F, red fox. 


THE dog: its domestication and behavior 

1 I 1 




. o 
’ci o 

^ P4 
^ K 









I I I 






2 : 



Q O 

I I 

^ Q 



§ -2 I 

<>i « o 

1 I 

I: I I 

O a: 5 u 

uoi9$!ua pimos ;sjy 



I I 

I I I 

1 1 


1 I I 

I I I 

I I 

I I I 

I I 

¥ s? -s 

•Complex combinations of more than two sounds are also possible, e.g., cough -* 
click -* growl-scream 

‘’Includes abbreviated form — the yelp and yip. 

'D, domestic dog; w, ,wolf; c, coyote; f, red fox. 

•‘Howl preceded by whining in wolf and yipping in coyote but not strictly mixed. 

Vocalizations in Wild Canids 


Figure 3. (A) Complex long grunt of a i -day-old female 
Chihuahua. (B) Yelp of a lo-day-old male Chihuahua (O Tran- 
sitional bark-yelp of a 2-week-old male Chihuahua. (D) Bark of a 
5-week-old male Chihuahua. <E) Sharp yelp with some vertical 
Stratification (final segment) of a i-day-old male Ins se 
Doberman pinscher. (F) Whine with coo component of a 26-day-ol 
male Irish setter x Doberman pinscher. 

ce of these souirds at birth, survival of the pups could be err- 

" Mfday of age, the Chihuahua may a sound^wWch^is 

St described as an extended grunt. , a Wt is wide- 

e sound is more complex than the grunt ( ^ „ when the 

nded with several frequency variaHons and occurs when 

imal is handled. . . j freaucncv 

By day 6 the pup's vocal capacty 
nations increase. At day lo sharp freque 

undingmost Uke a yelp. approximates those of the 

m and frequency range of the nse PP , . may 

lly developed bark. Thus, .t f,rrf,*k Furth^erLidcnce for this 

a developmental precursor of the bark, rur, 

mes from an intermediate stage weeks of 

hich can be heard (or better, seen spcctrograph.cnll) 1 at . 


THE dog: its domestication and behavior 

fear and aggression may concurrently display facial and body 
characteristics expressive of both motivations (Schenkel, 1947). The 
accompanying vocalizations are likely to include components that 
may be heard separately in pure form in fearful and aggressive 

Tables II and III indicate the mixed sounds that have been posi- 
tively identified, and it is likely that further investigation will reveal 
more sound combinations.* (See also Figure 2.) 

Less social canids such as foxes do not mix sounds to as great 
an extent as do the more gregarious canids (see Table II and IH). 
Foxes tend to live solitary lives and coming together briefly during 
the mating season; thus much of their vocal communication relies 
on calls that must be audible over long distances in order to be 
effective. Since these animals spend relatively little time in social 
units, a refined, graded system of low intensity vocalizations 
would have low selection priority. Gregarious canids such as the 
wolf and dog, however, tend to mix sounds more than the solitary 
canids, and facial and body expressions are also more highly dif- 
ferentiated (Fox, 1975). Thus, with increasing social complexity in 
the Canidae, there is also an increasing complexity of the com- 
munication repertoire. 


We have recorded developmental sequences for two domestic dog 
breeds: Chihuahua and Irish setter X Doberman pinscher. Data on 
the sound development of the red fox are available in Tembrock 


The Chihuahua can whine, scream, grunt, and mew at birth. 
All of these sounds are functionally similar as they serve to alert the 
mother to the distress and location of her pups. Without the pres- 

Vocalizations in Wild Canids 



The 12 sound types presented here represent an attempt to classify 
the major components of a complex vocal communication system 
in Canidae. 

Developmental data indicate that the earliest sounds present 
in canids are those which elicit approach of conspecifics, specifi- 
cally the mother. These sounds serve to decrease social distance. 
Once this distance is decreased, the mother may become aware of 
the needs of her young and may then serve these needs. On sev- 
eral occasions while recording the sounds of neonate domestic 
dogs, the mother was visually isolated from her pups but well 
within hearing range. As soon as the pups began to vocalize their 
distress to various experimental conditions, the mother made 
vigorous attempts to physically contact her young. Thus it seems 
that the distress calls (e.g., whines, screams) are releasers for some 
maternal behaviors, particularly retrieval. The w^ m w c e 
releasing mechanism works is unclear, but it may be possi e a 
the mother is (hormonally) predisposed (or sensitized) to tnfe^re 
these sounds as noxious/aversive stimuli and acts m su a y 
to cease them. „„ 

A similar interpretation may be applied to some 
calizations. Captive coyotes have been observed emi ng g 
screams when threatened at a distance by domman . 

had previously attacked them. The defensive ° • 

to cut off the attack. Here, again, the sound may be aversive or 

noxious stimulus to the dominant animal. 

The second set of sounds to develop are 
withdrawal of conspecifics increasing soa 

sounds (e.g., barks, growls, cUcks) are not^^^ 

develop between a and 4 weeks of age. A . _ pYolore their 
becomfng more self-sufficient -d ^ ^nmng ‘o ejlomjh 

tfte brradly dass^ cai^voca^s as ‘hose 


THE dog: its domestication and behavior 

age, when differentiation and mixing of sounds begins to take 
place. By about the 4th week of age, the development of the bark is 
complete (see Figure 3B, C, and D). 

At day 18 a clear successive emission of a mixed bark-growl 
may be heard. By the 4th week this combination of sounds be- 
comes more refined. 

Irish setter X Doberman pinscher 

As in the Chihuahua, whines, screams, gruntsi and mews are 
present at birth as distinct sound forms. At day 1 the sharp fre- 
quency rise (yelp), appearing at day 10 in the Chihuahua, was 
noted. In addition, some vertical stratification is visible from the 
spectrograph (Figure 3E), indicating a possible relationship to the 
growl. By day 5 frequency variations become greater. The first fully 
developed bark was noted on day 10. Mixing also begins to occur 
widely on this day as successive emission of sounds begins. Muting 
by superimposition begins between the 2nd and 3rd week of age. 
On day 26 a call was recorded when a pup was isolated. Spectro- 
graphic analysis later identified the call as having the short vertical 
frequency changes typical of the coo call of foxes. Cooing, how- 
ever, is not heard in dogs in its pure form, and this recording may 
provide further evidence for the evolutionary link between foxes 
and domestic dogs (see Figure 3F). 

Developmental data indicated that domestic dogs begin to mix 
sounds first by successive sound emissions and later by superim- 
position. The Chihuahua seems to develop its vocal repertoire 
somewhat more slowly than the mixed breed of Irish setter X 
Doberman pinscher. It should be noted that Doberman pinschers 
have been specifically bred as guard dogs, and the sooner they 
begin to vocalize the sooner they may be put to use. In addition, 
the Chihuahua has been bred for neoteny, a state of somewhat 
retarded development, and its schedule of vocal ontogeny may 
thus have been affected to some degree by the domestication pro- 

Vocalizations in Wild Canids 


Successive bark-howls and short rolling howls comparable to a 
barking stanza associated with defensive aggression in the wolf 
have been recorded. This is interpreted not as an evolutionary 
relationship between barking and howling but rather as a species 
typical phenomenon, where howling in the wolf (like barking in 
the domestic dog) may be at a low threshold and be evoked in a 
variety of different contexts. 

In addition to the A-eliciting and W-eliciting sound classes, 
Tembrock (1968) suggests two further sound groups: warning 
sounds and infantile sounds. The warning sounds (e.g., bark) 

serve as an alarm call for the entire social group. Rather than in- 
creasing social distance between members of the group (as with 
W-type sounds), these sounds tend (potenhaUy or actually) to in- 
crease the entire group's distance from an external danger. These 
sounds often occur in the defense of group territoiy or when one 
animal alerts its group members to a nearby predator. 

The infantUe sounds are those which have become denved 
and emancipated and reoccur in adulthood. The mewing sou no 
adult foxes is one possible example of such a denve voca iz , 
as is the yelping of adult dogs (see later). The former yoca iza 
occurs first in the neonate and serves to 

giving behavior and later reappears during courts ip an ‘ ^ 

Figure 4 further iUustrates the relaHonship of ng ^d 

W-eliciting sounds when viewed with respect to e ‘ intense 
of moHvaHon. As moHvaHon for approach 

A-type sounds may be emitted. Similarly^ as ^ emitted, 

drawal increases, more intense W-type soun . ^ gpd 

Certain sounds, however, cross over "e 

may be heard in either A-eliciting "^' 77 * .' nn Screaming, for 
sounds occur at the higher levels of mo ''“I ‘ 

example, may occur either as an mtense cojy a 

threat vocalizahon m foxes. An an g sounds such 

might be the observation that when hig jpp.irently m.ip- 

as laughing or crying may cross over a 

propriate contexts (Danvin, 1873). _,„HoMcal cons«iuences 

The group howl in wolves can ha p. ■ lopi-ltu r 

It is clearly an A-eliciting sound, 8 7 nd ac.oe 

for its duration and being prece c .wrox lurib) Oncer- 
submission-a coming together gre-etmg (Fox. .07 


THE dog: its domestication and behavior 










Increasing intensity/arousal 

W-eli citing 






Barking stanza 

Hypo»ie//cii; relationships between approach- and 
mIhdrawl-eUatmg sounds and increasing intensity tarousal 
Paradoxically, screams, with intense arousal, may be noxious 
(W-ehating) or atlenlion/care-soliciting (A-eliciting). 

come evident (see Figure 4). Considering first the A-tvpes the 

Ih^DDroa'^ch'^ T ‘ expression of a moHvation/need for 

the approach of a conspecific. The more intense versions of this 

HTt"scr:3r''1'in^ whine, "eirand con! 

spoctrographically. ^ ^ features may be seen 

inten^^ocMexnrn ^e the least 

iy-se social 

^\V-^vr»n^ + 1 • point ol the second conhnuum 

•nd ddife™ b,„ki„g p„|p„|.,; ™„ a" 

Vocalizations in Wild Canids 


indicate that some type of social reinforcement or facilitation is 
involved in achieving full vocalizing potential. 

The fact that squirrel monkeys deafened at birth are capable of 
producing all normal vocalizations indicates that the vocal reper- 
toire is largely genetically predetermined. This seems to be the case 
in domestic dogs as well since experiments by Fox (1971a) indicate 
that no auditorially evoked potentials could be recorded from the 
dog's brain until 2 weeks of age. In effect, the dog is deaf until this 
age; but vocalizations begin to develop at (or possibly before) birth, 
and the basic sound repertoire is complete by about 4 weeks of age. 

In addition, hand-raised domesHc dogs fed and handled on a 
strict schedule quickly decreased their frequencies of care-soliating 
distress vocalizations, presumably because their sounds were in no 
way positively reinforced by petting or feeding (Fox, i9^a). 

When placed in unfamiliar surroundings, domestic dogs gen- 
eraUy directed contact-seeking sounds toward the 
often barking, whining, and yelping, while wld canids 
be silent. This supports other evidence that there may be a geneh 
predisposition toward dependency in the dog whic is no prese 
in wild canids (Fox, 1971b). .c 

Barking is another sound form which is of 
it seems to have hypertrophied in the domestic og 
used in a much greater variety of contexts than among w 
As Table I indicates, dogs may bark dunng play 

soUdtlng, threat, defense, _soficiting 

and yelp-barks. This contextual vanety 

itself may not always convey °™rific infoniiation to 

tracts the attention of the receiver. The m P l ^_pJ5 

follow would then be received through other 

visual and/or olfactory. These cues ^vould then ident.f) the mean 

ing of the accompanying barks. distinction 

From the inventory of various sou . .u vuloine and 

can be made between foxes The similarities 

canine subgroups of the genus Cfliiis mg taxonomic 

betxveen wolf, dog, and dine oHhc origin(s) of the 

affinities but add little to our understanding 01 b 

dog prior to domestication. The outstanding feature 


THE dog: its domestication and behavior 

tain occasions, however, the group howl may be aborted and ag- 
gressive behavior may be released. This has been observed upon 
numerous occasions in captive wolf packs and also among captive 
groups of coyotes. A tape-recorded howl or a siren may be used to 
evoke group howling, but at the point of coming together, any 
conflicts present between group members may be reactivated as a 
result of the ensuing close proximity. 

A particular facial expression, open mouth "play face," 
coupled with panting in the domestic dog may be analogous to 
laughter in man (Fox, 1971b) occurring in similar contexts, namely 
greeting and play-soliciting. In the red fox, panting may be accom- 
panied by muffled screams, mews, and purring sounds during 
greeting.^ The excited panting, a metacommunicative play signal, 
exeniplifies how emotional changes may influence the rate and 
depth of respiration. 

data, particularly that concerning mixed sounds, imply 
that canid vocal communication is essentiaUy an emotional lan- 
page, comparable to the intenHonality expressed in nonvocal 
body postures and facial expressions. This is supported by the fact 
gradaHons of sound types are possible indicating 
he degree of arousal motivaHon and intentions in a given context 

tonerof ‘o ‘he "paralanguage” or e^tional over- 

l^mt moHvT " “"•espond to mixed or ambiv- 

thafZT^ 1^"® f Experiments by Tembrock (1958) indicate 
is more f =^P^™‘ed from their mother 

throWKcT ‘he mother's retrieval behavior than 

lendfsuDoo^ themselves. This, ton, 

sdd thaTfs ‘‘ “ "^“ssarily so much what is 

said that is of signihcance but rather how it is said 

less frequently than those raised with conspecifics When intro- 
duced at a later age to other animals, howeven these isXes beean 

WiZT ^t'" f “f 1 ‘hose raised in sodal groups. 

Winter el a! (1973) report the same phenomenon in fquinel 
monkeys (Saimm ^„rc«s) which had been deafened at bWh or 

of vSn^ r ‘hoh frequencies 

of vocalizing when introduced to conspedfics. These observations 

Vocalizations in Wild Canids 


Developmental data indicate that domestic dogs first begin to 
mix sounds by successive sound emissions at about 10 days of age 
and later by superimposition between 2 and 3 weeks of age. The 
frequency of occurrence of the basic sound types in different con- 
texts varied between species but not within species. The possible 
effects of domestication on canid vocalizations are discussed. 

Vocalizations in Wild Canids 


Developmental data indicate that domestic dogs first begin to 
mix sounds by successive sound emissions at about 10 days of age 
and later by superimposition between 2 and 3 weeks of age. The 
frequency of occurrence of the basic sound types in different con- 
texts varied between species but not within species. The possible 
effects of domestication on canid vocalizations are discussed. 

Vocalizations in Wild Canids 


Developmental data indicate that domestic dogs first begin to 
mix sounds by successive sound emissions at about 10 days of age 
and later by superimposition between 2 and 3 weeks of age. The 
frequency of occurrence of the basic sound types in different con- 
texts varied between species but not within species. The possible 
effects of domestication on canid vocalizations are discussed. 


THE dog: its domestication and BEHAVIOl 

tic dog — balking — ^may be attributed to artificial selection. A go( 
house dog barks at intruders. Barking in all wild canids similai 
serves as a warning or threat to intruders (except during grot 
vocalization) and is context specific. Is the lack of context specifici 
in the dog a hypertrophy of domestication, or does it point to a ve 
different nonwolf canid ancestry? Surely it would be of little adva 
tage (to man) to selectively breed dogs that bark with virtually i 
context-related specificity, although it would be most difficult 
exercise context-specific selection. An alternative view is that tl 
selection pressure for silence necessary in a wild predator has bei 
relaxed. This, coupled with a high degree of dependency and var 
ing degrees of neotenization or infantilism with care-soliciting b 
havior and vocalizations in adulthood directed toward the owne 
would suggest that both domestication and socialization early in li 
have a profound influence on the dog's vocal repertoire. The oi 
gin(s) of the dog therefore still remains an enigma although oi 
might conclude on the basis of this study that if the wolf were tl 
sole progenitor of the dog, then dogs would howl more and ba: 
much less than they do. Dogs also yelp in many different contex 
compared to other canids. TTie prevalence of this sound may ind 
cate a clear taxonomic difference between species. Another accep 
able interpretation is that the yelp, an infantile sound, persists in 
maturity and occurs frequently in distress/attention-seeking coi 
texts in dogs because of the dependency promoting neoteny i 
infantilism induced through domestication (since the more depei 
dent the dog is, the more trainable it is) (Fox, 1972). 


On the basis of speclrographic evidence, it has been possible I 
identify 12 basic vocal sound types of canid species. 

Vocalizations may be mixed by successive emission of two < 
more sound types, by superimposition of these sounds, or by 
combination of these two forms. The same basic sound type ma 
differ among canid species along the dimensions of sound dur; 
lion, separation time between consecutive sounds, principal frt 
quencies, cyclicity, and context. 

Vocalizations in Wild Canids 


Developmental data indicate that domestic dogs first begin to 
mix sounds by successive sound emissions at about 10 days of age 
and later by supeiimposition between 2 and 3 weeks of age. The 
frequency of occurrence of the basic sound types in different con- 
texts varied between species but not within species. The possible 
effects of domestication on canid vocalizations are discussed. 


Behavior Genetics of 
Fi and ¥2 Coyote x 
Dog Hybrids 


This study represents an interim review of the behavior and 
morphological features of F , and Fj coyote x beagle hybrids. Earlier 
studies by Silver and Silver (1969) and Mengel (1971) are lacking in 
detailed analysis of the behavior of parent stock, notably of the 
fixed action patterns which to the ethologist can have as much 
taxonomic value as morphological features to the comparative 
anatomist. Several species-typical action patterns have been iden- 
tified for the coyote (Cam's lalmns) and for the beagle (Cams 
familiaris) in our laboratory and quantified ontogenetically in sev- 
eral animals (Fox, 1969a and b, 1970, 1971a and b; Fox and Clark, 1971; 
Bekoff, unpublished observations). The purpose of this section is 
to present an integrated overview and to discusss some intriguing 
findings which have not as yet been considered. 

Materials and 

Developmental data were obtained from 4 male and 4 female 
beagles, 6 female and 4 male coyotes, and 16 F. coyote x beagle 

9 ' 

9 ^ 

THE dog: its domestication and behavior 

hybrids, 6 of which were females; of this group, which comprised 
six litters, 2 males died prior to weaning. Two male and two female 
F, hybrids were obtained as adults and no ontogenetic data were 
available for these animals which were bred by artificial insemina- 
tion (courtesy of Dr. J. J. Kennelley, Bureau of Wildlife and 
Fisheries, Denver, Colorado). All subjects studied developmentally 
were hand-raised by stomach tube on Esbilac®, a synthetic bitch's 
milk formula (Borden Company). The various morphological and 
behavioral characteristics listed in Tables I and II were looked for. 
Much of the behavioral data were collected from dyads interacting 
between 21-50 days of age and subsequently from groups of ani- 
mals housed in groups of three or four. The most significant find- 
ings to date are reviewed (see Figure 1). 



All Fi hybrids had flop or pendulous ears, bushy coyotelike tails 
with an active supracaudal gland. Dewclaws were absent. The body 
type of the F ,'s is best described as mesomorphic, being stockier 
than the coyote, but lighter and leggier than the beagle. All F, 
hybrids had a smooth coat with guard hairs slightly longer than the 
beagle but shorter than the coyote; the winter underhair was much 
thicker than in the beagle. (See Table 1 and Figure 1.) It should be 
added that two of the Fj canids, both with piebald coloration, had a 
medium (coyote) length coat that was broken rather than smooth. 
The remaining 12 Fj hybrids had coats intermediate in length and 
with underfur density between coyote and beagle, but all coats 
were smooth like the beagle (Table I). Their coat color varied, being 
dark sable in the winter and paler in the summer. 

The Fj generation showed independent segregation of beagle 
and coyote characteristics (see Table I). Erect ears, a coyote charac- 
teristic, were less frequently seen than pendulous or semipendu- 
lous ears. All animals had fairly bushy tails and two had dewclaws 
on the hind legs. The piebald coat color (white and brown/black) of 
the beagles was seen in a low percentage of Fj's, most of the ani- 

Table I. 


Behavior Genetics of Coyote x Dog Hybrids 


S3UXU03 /uojoduof 

idddn Jo uoijdruj 



fZ JZ ^ ^ c 

I B- ^ S' S 

r*. o w o ^ 

(iJ 6 S £ S 

3}auo9u jyjpQ 

(s8a] puiii) SrtiopflWQ 
puviS ppi patfoy 
iwt /fi/sng 
s /03 dojj 
S /03 P 3 J 3 -IIM 35 


o i 5 


sp^fqns Jo joquintq 



•Sc.iwnal v.inations from pale lo dark coat color. 
PiRures denote numbers amma^s. 

Behavior Genetics of Coyote x Dog Hybrids 


mals being either pale or dark sable without any large areas of 
white on the body, although most F^'s had white around the muz- 
zle and lower jaw (i.e., white facial mask of the coyote) and also on 
the tail tip. The dark sable type tended to develop a pale coat in the 
summer months like the F, hybrids (see Figure 2). The most fre- 
quent somatotype was a long-legged coyotelike ectomorph, al- 
though a smaller percentage of endomorphs, which were stockier 
and sometimes shorter-legged than the beagles, were seen. The tail 
gland odor was harder to detect and seemed less active in the 
beaglelike Fj's compared to their ectomorph littermates. These 
endomorph-type hybrids also had an overwhelming "doggy" 
smell, much stronger even than in beagles. 

Eruption of the upper temporary canine teeth in the Fj canids 
was usually earlier than in the beagles, the age of eruption being 
extremely early in the coyote compared to the domestic dog 
(Table 1). 

One of the most intriguing morphological characteristics was 
the neonatal coat color, the significance of which is discussed sub- 
sequently. All wild canids are dark at birth (Fox, 1971b) and do not 
possess the adult coat color, while most domestic dogs show the 
adult color at birth. The majority of the F2 hybrids had a dark 
dusty-brown neonatal color, which eventually gave way to a pale 
or dark sable. Two animals (Table I) had the adult color at birth, 
namely the beaglelike piebald coloring. 


Both the F, and Fj hybrids were timid and shy of strangers. The 
endomorphic beaglelike Fj's were less timid than the more ec- 
tomorphic coyotelike Fj's. (See Figures 3 and 4.) Coyotes, even after 
being hand-reared, become increasingly shy of strangers with in- 
creasing maturity (Fox, 1971b). The wildness of these canids, or 
capacity to regress to a feral state, was acddentally evaluated at our 
field station. Two Fj hybrids and one beagle escaped from their 
enclosure; the latter animal stayed close to the enclosure and was 
easily caught, while the hybrids, both ectomorphic or coyote types, 
roamed the 2000-acre station for several days before hunger 
brought them back and they could be coaxed back into the pen 

Behavior Genetics of Coyote x Dog Hybrids 


with food. Three similarly raised coyotes of the same age were re*- 
leased at the field station and were provided with food at the spot 
where they were released. They moved away permanently from this 
site after 4 days, and were not seen again. 

As in wild canids, the first signs of shyness toward novel 
stimuli (environmental fear) began to develop around 5 months of 
age in a high percentage of the F2 hybrids. The wild temperament 
trait is discussed in detail earlier (Fox, 1971b). 

Both coyotes and Fj hybrids showed marked aggression to- 
ward members of the same sex (Table II). Fj hybrids also showed 
increasing proximity intolerance for members of the same sex, al- 
though unlike the coyotes (Fox and Clark, 1971), they did not fight 
seriously between 4 and 5 weeks of age. Dominance fights oc- 
curred later, around 6-9 weeks, and permanent hierarchies were 
formed shortly after this age. By 6-8 months, intrasexual aggres- 
sion was marked and was the cause of death of one subordinate 
male F* hybrid that for necessity had to be housed with male and 
female littcrmates. 

Clasping a conspecific around the waist during aggre‘;sive in- 
teractions (Fox, 1969b), a typical action pattern occa'^ionally ob- 
served in the beagle, was fret]uently seen m lxitli_F, and F, hvbnds 

Figure 3. Agonistic interactions in coyotes and Fj coyote X 
beagles, (a) Intense intraspecific aggression and high proximity in- 
tolerance in 29-day-oId coyotes; (b and e) defensive threat gape in 
coyote and hybrid; (c and d) more submissive-defensive gape in Fj 
hybrid, similar to coyote (ft. See facing page. 

Aggressive displays in the coyote include horizontal extension of 
the tail, while in the beagle it is arched in a more vertical position 
(Table II). In the Fi hybrids, both tail positions were seen, and often 
a compromise tail position, between the vertical and horizontal, was 
observed during agonistic encounters. F* hybrids showed both 
coyote, beagle, and intermediate typo tail positions, the vertical 
position occurring in the beaglelikc endomorphs and the horizon- 

tal position in the ectomorphic types. The latter hybrids more often 
showed the intermediate position than the former, and the tail at 
rest was held down as in the coyote. 

Threat-gapes (Fox, 1970) and hip-slams (Fox, 1969b) are action 
patterns common to the coyote during agonistic interactions and 
have not been observed in beagles. Both actions were seen occa- 
sionally in the F, hybrids at lower amplitude and frequenc)'; F; 
hybrids showed a greater range of variation in occurrence of the 
threat-gape (Table II), but all showed the hip-slam during fighting 
and play-fighting. 

The prey-securing forelimb stab and ability to catch. Kill, dis- 
sect, and ingest live prey (4-week-oId rats) will be quantifed in 
detail in Chapter 6. Most F. hybrids exhibited the forelimb stab of 
the wild canid, and the majority of these animals were efficient at 
killing and ingesting prey. Those that failed (interestinglv. the 

Figure 4. Action fxittcnis typical of coyote in F* coyote X dog hy- 
brids: (A) standing-over, (B) threat-gape. (C) inguinal response 
(hind leg is raised). 

bcaglct>T3e endomorphs) in executing a normal coyote-killing se- 
quence showed inhibition of the prey-killing bite, so that injured 
prey were eaten alive. In coyotes, no bite inhibition was observed, 
while in beagles, bite inhibition, plus inhibition of eating, w'cre 

Tnble II. 


Behavior Genetics of Coyote x Dog Hybrids 



s fv 

qpis quiji^joj 


iwi 9<itss^jSv 


}ivi MissyjSSv 






fimupjMiiujfi ^ 1/5 
sp.flqfis /<» 


THE dog: its domestication and behavior 

The inguinal response, a display of considerable ontogenetic 
and social significance in Canidae (Fox, igyid), occurs rarely in 
beagles but consistently during social interaction in coyotes. This 
display was seen in both Fi and hybrids (Table II). 

During friendly sodal approach, the more social canids, such 
as dogs and wolves, show a licking intention, often combined with 
a submissive "grin" (Fox, 1970). In coyotes, this licking intention is 
rarely seen and at low frequency. A slightly higher frequency was 
noted in the Fi hybrids and in some individual Fj's; in the latter 
there was no apparent correlation with the somatotype. 

Estrus in the coyote occurs in early spring (February) so that 
the birth of cubs is timed with a relative abundance of prey. In the 
beagle, there are two heat cycles per year, usually in the spring and 
fall (but in many individuals at alrnost any month of the year). 
Estrus in the F, hybrids was restricted to late fall-early winter. The 
Fj hybrids were more variable, estrus occurring at any time from late 
fall to spring; only one heat was recorded during the summer. One Fj 
animal had two heats (spring and late fall), but no fertile mating 

As early as 3 weeks of age, a marked difference in response to 
handling was seen in Fj hybrids. Some pups felt more tense and 
had a greater muscle tone characteristic of infant coyotes, while 
others remained relaxed, almost flaccid, when picked up, like beagle 
pups. There was no correlation vrith these two types and their 
somatotype. The more tense pups were more easily alarmed by 
sudden noises and would invariably give an open-mouth threat- 
gape which is first seen at this age and similarly evoked in coyotes' 
(Fox, 1970). An effective, although unsophisticated, test for pain- 
induced aggression first used in studying individual differences in 
coyote cubs was used on these hybrids. The test consisted of hold- 
ing the cub in one hand, abdomen uppermost, and with the other 
hand alternately and mildly pinching the cheek skin. In the relaxed 
hybrids, there was either distress vocalization or no response. The 
tense hybrids reacted like coyote cubs ivith defensive threat-gapes 
and at a later age (4 weeks) with growls and vertical retraction of 
the lips. Repeated stimulation (10-15 times) would produce a 
ragclikc reaction and self-directed aggression where the subject 
would seize and bite one or both of its forepaws. This had a vicious 
circle effect, self-inflicted pain increasing the aggression. Movies 
taken of these two different sets of reactions dramatically illustrate 

Behavior Genetics of Coyote x Dog Hybrids 


this phenomenon, which may be attributed to threshold dif- 
ferences in responsiveness to mild cutaneous stimulation. One of 
the tense hybrids at 4 weeks of age had to be forcibly restrained 
and the canine teeth clipped, after a brief fight with a conspedfic 
which triggered self-directed biting; it was unable to walk for sev- 
eral days, both forelimbs being severely mutilated. No such ex- 
treme reactions (low threshold?) have been observed in coyote 

The pups identified as tense individuals at 3-4 weeks were 
generally more efficient in handling live prey, showed less prox- 
imity tolerance and greater intrasexual aggression, and were actu- 
ally dominant over their relaxed conspecifics. Future studies will 
attempt to quantify such early individual differences in respon- 
siveness to cutaneous stimulation. 


The majority of F2 hybrids had a characteristic defect in that the tip 
of the tongue often protruded out of the mouth while at rest. 
Measurements have not been taken, but this may be either a neuro- 
logicaJ defect or a disproportion between tongue and muzzle 
length. When alert, all but z of the 14 F2 hybrids could completely 
retract the tongue. This anomaly was not seen in the Fj hybrids. 

The endomorphic F2 hybrids also showed varying degrees of 
prognathism, the lower jaw being shortened. Dentition appeared 
normal and in no instance was the malocclusion severe enough to 
interfere with the alignment of the permanent teeth. 

All endomorph beagletype Fj hybrids had a delayed closure of 
the parietal fontanelle (4-6 weeks). Like beagles, these latter ani- 
mals were more vocal than the ectomorph type. The Fj's had simi- 
lar vocalizations, namely a bark-howl which, as in the F, hybrids, 
sounded like a successively combined beagle and coyote call. 


The morphological and behavioral data strongly suggest that the 
follovving traits have a dominant mode of inheritance: bushy tail. 



pendulous ears, sable wild color, short guard hairs and smooth 
coat, seasonal change in coat color, active supracaudal gland, dark 
neonatal coat color, coyote while facial mask (around lower jaw 
and muzzle), coyote ectomorph somatotype, one annual estrus, 
intrasexual aggresslvity, aggressive clasping, hip-slam, threat- 
gape, inguinal response. 

The dark neonatal coat color, a characteristic of all wild canid 
species so far studied (Fox, 1971b), may be related to heat conserva- 
tion since neonates are partially poikilothermic. Most domestic 
breeds of dog have the same coal color at birth that they will have 
as adults, though a greater number show a seasonal change in coat 

Eruption of the upper temporary canine teeth, which is very 
early in wild canids compared to all domestic species so far studied, 
was earlier in both F, and Fj hybrids. As in the beagle, erup- 
tion of the lower canines occurred later in the Fj hybrids, and the 
upper incisors erupted earlier than the lower, the central pair usu- 
ally being the last to emerge. As would be predicted on the basis of 
independent segregation of the Fj's into beagle meso/endomorphic 
and coyote (ectomorphic) types, tooth eruption was earlier in the 
coyote type. 

Mengel (1971) also noted a greater variation in Fj hybrids from 
doglike to coyotelike compared to the more intermediate F, hybrids. 
However, he did not report any detailed developmental data, but 
it is significant that all his hybrids were aggressive and fought a 
great deal early in life. A similar increase in aggression, compared 
to the beagle, was apparent in all Fi and F^ hybrids in the present 

Mengel reported small litters from the F, hybrids, and this 
corroborates the present findings where the average litter size was 
2.7. This may be indicative of a lower fertility in these hybrids. 

Gier (1975) and Mengel (1971) have both remarked that shift in 
timing of estrus in coyote x dog hybrids would prejudice survival 
of any offspring bom in the wild during the winter (except in 
temperate southern regions of the United States). These data add 
further weight to their argument. Kennelly and Roberts (1969), in a 
study of the F, hybrids used in this study, found evidence for 
seasonal spermatogenesis in the males. 

The inguinal response, a highly ritualized social display in 
coyotes which has a clear ontogenetic history (Fox, (1971b), was also 

Behavior Genetics of Coyote x Dog Hybrids 


seen at high frequency in the Fj hybrids but only rarely in beagles. 
Its function early in life may be to truncate agonistic interactions 
prior to the establishment of social relationships. The high fre- 
quency of this display correlates with the great incidence of fight- 
ing during the first 3-5 weeks of life in both coyotes and Fj hybrids 
compared with the beagle. 

Behavioral and developmental studies of these canid hybrids 
have made it possible to identify a number of behaviors which, as 
emphasized earlier, may be as valuable as morphological traits in 
facilitating the identification of patterns of inheritance and of pos- 
sible ancestry. Of particular interest and a focus for future research 
on subsequent generations and back-crosses is the ontogeny of ago- 
nistic behaviors and quantitative analysis of various displays and 
action patterns. The canid family holds a wealth of possibilities for 
further studies of behavior genetics since many spedes (wolves, dogs, 
coyotes, and jackals) (Gray, 1954; Kolenosky, 1971) will hybridize, 
and for each of these spedes, characteristic action patterns and 
displays have been identified and detailed ethograms and devel- 
opmental data are available (Fox, 1971b). 


The frequency of occurrence of various morphological and 
havioral characteristics are documented in coyotes, beagles, an 
their F, and Fz hybrids. These data reveal certain consistences in 
the patterns of inheritance of such beagle traits as pendulous ears, 
smooth, short coat; and coyote traits, such as ectomorp y, sa e 
coat color, dark neonatal coat color, bushy tail with active supra- 
caudal gland, and white facial mask. The above traits were most 

frequently seen in the F2 hybrids, while the Fi hybn ^ ^ 

intermediate between the dog and coyote and extreme T 
in appearance. In the F^ hybrids, independent 
apparent, most offspring being coyolelike ectomorp ® ^ 

dulous or semipendulous ears, while others were S 
domorphs, but with proportionately shorter legs an f 
than actual beagles. Both F. and F= hybrids resembled the coj me m 
terms of shyness, intrasexual aggression, an interaction 

action patterns associated avith aggression and soci. 


Effects of 
Domestication on 
Prey-Catching and 
Killin g in Domestic 
and Wild Canids and 
F2 Hybrids 


Following earlier developmental studies of prey-catching and kill- 
ing behavior in various species of Canidae (Fox, (1969a), the pres- 
ent investigation focuses upon differences in organization an 
temporal ordering of these behavior patterns in coyotes, beag^s, 
and F, and F, generation coyote x beagle ("coydog ) hybnds The 
objective was to determine what effect, if any, dornestication nuiy 
have on prey killing in wild and domestic canids an t cir ) 

This investigation is dii-idcd into two parts, the first dea mg 
with more qualitative aspects of behavioral organization and em- 
poral ordering or sequencing and the ^econ "i u 

malysis of two action patterns, the vertical leap and the forehmb 
stab. (For detailed descriptions of these action pattims, see ■ . 

1969 and 1971b.) 


io8 THE dog: its domestication and behavior 

Materials and 


In the qualitative part of this investigation, subects were 8-9 weeks 
old when tested and had no prior experience with live or dead 
prey. Differences in behavior might therefore be attributable to 
genetic rather than experiential influences. The temporal ordering 
of action patterns and the frequency of certain action patterns were 
recorded for qualitative and quantitative analysis, and tests were 
repeated in order to determine what effect experience might have 
on subsequent prey-catching and killing behavior. Additional 
studies were made on six coydogs in order to evaluate the possible 
Influence of experience in the test/retest design of the experiment. 

Four beagles (littermates), 9 Fj (from 3 litters), and 8 Fj (from 3 
litters) generation beagle x coyote hybrids and 13 coyotes (from 3 
litters) aged 8-9 weeks were used in this study. They were hand- 
raised in incubators from 3-6 days of age, being fed regularly on 
Esbilac via stomach tube, as described by Fox (1966). This method 
was chosen to control for individual differences in maternal be- 
havior. All subjects were raised indoors in pairs or trios and had no 
exposure to live or dead prey prior to testing. They were never fed 
fresh meat and were raised on commercial dog food (Purina Chow 
and Gaines Burgers) being weaned at 3 weeks of age onto this 
food blended with Esbilac and housed in littermate groups in 4 
X 10 ft cages. Each subject was carried from the animal room into 
the soundproof testing room opposite and was then observed 
alone in a 5 X 5 ft arena, where the prey, a 4 to 5-week-old white 
rat, was placed. This type of prey was chosen for convenience, 
being readily available and having been used consistently in earlier 
studies with canids. An arbitrary cutoff time of 20 min was as- 
signed for each test, during which all behavior was recorded 
against a time-base using world-symbols and abbreviations for the 
various action patterns (see Tables I-III). It was then possible to 
quantify the frequency of certain action patterns and to trace tem- 
poral sequences of prey-catching, killing, dissection, ingestion. 

Effects of Domestication on Prey-Catching and Killing 


and play with prey. If the subject did not kill and/or eat the prey 
during this 20 min period, the prey was killed immediately after 
the test and was presented to ^e subject with the abdomen cut 
open to expose the liver and viscera, and observations continued 
for a maximum period of an additional 30 min. If the subject gave 
no response after 5 min, the liver was removed and placed in its 
mouth in order to sensitize the subject to the carcass. This is occa- 
sionally effective in stimulating a naive canid to eat prey for the 
first time (Fox, 1969). The action patterns associated with dissection 
and ingestion of the prey were recorded until the prey was eaten or 
partially eaten and ignored. This time period varied up to approx- 
imately 30 min. 

All subjects were retested 24 hr later in order to determine 
what effects the first experience with prey had on subsequent or- 
ganization and sequencing of action patterns. 


From a qualita«ve study of prey-catching and kiUing in coyotes, 
beagles, and F2 generation coyote x beagle hybrids, it was observed 
that two very distinct action patterns were a consistent part of all 
three of the above species' behavior repertoire. These action pat- 
terns are the forelimb stab and the foreUmb stab with a vertical leap 
(see Figure 1). The latter is analogous to pinning down descnbed by 
Eisenberg and Leyhausen (1972) in other predators. 

It was felt that quanHfication of the frequency of the occur- 
rence of these action patterns in controlled observational situations 
might render an appropriate index of the degree to which these 
three species were aroused and moHvated to e lat these action 
pattern! The second section of this chapter, therefore deals specif- 
ically with quantified analyses of these particular behaviors. 

After completing the prey-kilUng tests at 9 u-eeks of age, t 
same litter of four beagles, hvo of the litters of six coydog hy- 
brids, and one of the litters of three coyotes, were kept for this 
study. Four beagles (littermales), six F, generation beag e x co> o c 
hybrids (littermates), and three coyotes (also littcmatcsk . 5 9 - 

weeks of age were thus used in this study. Each subject uas ob- 
served in the 5 X 5 ft .arena, the floor of which ivas covered bv a 


THE dog: its domestication and behavior 

Figure i. Vertical leap (a) followed by forelimb stab (b) directed at 
visually concealed prey by generation coyote X dog. 

Effects of Domestication on Prey-Catching and Killing 


white linen sheet. The edges of the sheet were secured under the 
plywood walls of the arena. The prey, two 4 to 5-week-old white 
rats, were placed in the arena under the sheet. The two action pat- 
terns (vertical leap and forelimb stab) were most often elicited 
when the canids observed the movement of the rats under the 
sheet. Each test was arbitrarily divided into two 10-min intervals 
(20 min for each test), during which the frequencies of these two 
action patterns were recorded. The total interaction time between 
canid and prey was also recorded. In addition, qualitative notes 
describing major events such as death of the prey and overt signs 
of degree of arousal of the subjects were also recorded. Each 
20-min test was repeated within a week after the initial test. 




In the four beagles tested, all subjects reacted toward the rat; 
but interactions were brief, and the rat would frequently be ig- 
nored as the dog suddenly began to investigate the arena or at- 
tempted to get out of the arena. These observafaons clearly imply 
that the beagles were less motivated than the coyotes and coydogs. 
No prey was kiUed in either the first or second tests. 

The following behaviors were recorded: onentation, approach, 
follow, investigation (sniffing and pawing), approac wi ' 

bite intention, Lse-stab, head-shake intenhon leap-leap foHowed 
by bite intention, nose-stab or head-shake intenhon P^mg 
■aese actions may be followed by an ,he 

sideways. Only one beagle contacted the live rat with 
prey being licked and gently nibbled with the incisors. All subjects 
showed plav-soUciting behaviors, including the bow, exaggerated 

and also barking and yelping 

■' '"LIL ....... «» 

patterns were observed, bite, carry, one 


THE dog: its domestication and behavior 

forelimbs, hold with one or both paws and bite. No dog killed the 
rat in the first or second tests. 

These observations show that although the dogs were at- 
tracted toward the rat, the duration of interaction (and therefore 
possibly the motivation) was much shorter than in coyote or 
coydog and a number of prey-catching and killing action patterns 
were absent. The normal canid temporal sequence of orientation, 
approach, investigation, bite, carry, bite (and head-shake) to kill, 
followed by dissection and ingestion was truncated at the bite in- 
terphase. Investigation was instead followed by self-play (chasing 
own tail), play-soliciting (which is not unusual in wild canids but 
which is normally satiated after 10-15 min), or by a bite intention. 
The dogs would lunge at the rat and bite in vacuo (air-snap) or 
deliver nose-stabs which were interpreted as bite intentions. Such 
actions were often preceded by forward leaps and followed by one 
or more backward leaps. This leap-leap-nose-stab sequence (see 
Table I) was only observed in the beagles and also occurred during 
intraspecific play. The same sequence of actions has been recorded 
in Chihuahuas, malemutes, malemute x wolf hybrids, and several 
domestic dogs of mbced breeding, but not in coyotes or wolves 
during intraspecific play. The possibility that this action pattern 
sequence is a specific marker lor Cams familiaris, as a species charac- 
teristic, should be considered.* 

When retested with live prey after 24 hr deprivation of food, 
only one of the four subjects showed no additional inclusions of 
the actions associated with the prey-catching and killing sequence. 
In one subject, the rat was bitten 13 times, and on each occasion the 
bite was inhibited, the rat being uninjured and active at the end of 
the test. The rat was grabbed and carried five times by this subject, 
and on the third carrying episode (15 min after onset of test) a weak 
head-shake occurred which was more violent on the fourth carry- 
ing episode but did not occur subsequently. This subject also made 
four low amplitude forelimb stabs at the rat during this second lest. 
In the first test, this subject directed neither biles nor forelimb stabs 
at the rat. Another subject added only two inhibited bites to its 
earlier repertoire. 

•More important though is the fact that this is an Inlraspcdfic action that was 
directed at the prey which, as cmphastied earlier (Fox, 1969), may be responded to 
as a play*objcct or partner in some canids until it is learned that the prx’y is food. 

Effects of Domestication on Prey-Catching and Killing 


Table I. 


Beagle Male II (First Test) 

No immediate orientation. 

2 min 

Then orients, rushes, paws, TW (tail-wag), sniffs, then ignores, 
then approaches, TW, bite intention, head-shake intention. 
Self-play leap-leap-leap-nose-stab. 

5 min 

Investigates then ignores rat. 

6 min 

Leap-leap-nose-stab, paws, chases, bite intention, investigates, 

7 min 

Licks rat's face. 

Paws, bite intention, play-solicits, TW. 

8 min 

Lunge, nose-stab, A/W (approach/withdrawal), play-solidts. 
Nose-stab, A/W, bite intention. 

20 min 

Play-solicit, bite intention, yelp-growl, TW. 

(Brief poorly sustained interactions — no clear bite, cany or 
forelimb stab.) 

22 min 


12 min 

Rushes, gently nibbles, paws, A/W, nose-stab, bite intention. 

TW, play-solicit, paws, yelps, leap-leap-A/W nose-stab, bite 
intention, yelp. 

14 min 

A/W, bite intention, TW. 

Leap-leap-leap-nose-stab, A/W, play-solicits. 

Leap-leap-leap away, bite intention, leap away. 

15 min 

Growl-howl-bark at rat. Play-soliciting dance— sustained playful 
interaction for last 5 min. 

(Rat is alive and well.) 

Beagle Female IJ (Retest) 

Immediate rush, paws, and iw/es, but bite inhibited. Then ignores 

2 min TW, bite — carry, then dropped in one comer. 

Inhibited bite, then bite intention. 

Yowl-barks at rat + nose-stab. 


THE dog: its domestication AND BEHAVIOR 

Table I. {continued) 

5 viin Approaches and mouths and leaps away. 

Leap-leap and mouths. 

7 min Mouths, leaps back, then bile intention. 

Plays with tail of rat. 


Play-soUdts + nose stab. 

n min Leap bile (inhibited). 

Paws and mouths. 

15 min Ignores rat, little interest. 

16 /nin Carries, drops, one forelimb slab. 

Carries, weak head-shake. 

Carries, strong head-shake. 

Drops, mouths, carries, mouths, drops, /orelimb stab. 

28 min Stalks and rushes, forelimb stab, growl. 

Bite intention. 

(Rat is alive and well.) 

A third subject showed a marked increment of actions, giving 
14 inhibited bites and 8 forelimb stabs and grabbing and carrying 
the rat 10 times. On the fourth carrying episode, piloercction oc- 
curred, and on the sixth episode (10 min after start of test) the first 
of three head-shakes, which subsequently increased in intensity, 
were noted. 

An interesting and bizarre coupling of action patterns was 
recorded after the second grab-carry episode, which occurred 8 
times. This was the inclusion of a high amplitude leap, which on 
the last three occurrences, was coupled with a head-shake but 
which occurred after the dog had leaped at, grabbed, and carried 
the rat. Instead of the usual temporal sequence of leap, grab and 
bite, head-shake and can)* (or cany and head-shake), this subject 
coupled the carr)* component with jin additional leap while it had 
the rat in its mouth. And on three later occasions when this mis- 
placed leap was seen, a violent head-shake was recorded simul- 

Effects of Domestication on Prey-Catching and Killing 


It is logical to propose that this prey-catching leap (while the 
prey was in the dog's mouth) was a misplaced component of a 
disordered temporal sequence and that it subsequently entrained 
the head-shake component which normally occurs after a leap 
when the prey is secured in the dog's mouth. 

When given dead prey with the viscera exposed after the first 
test, additional evidence of the dogs' inability to efficiently dissect 
the prey was obtained. Only one of the four subjects ignored the 
carcass completely. A second subject ignored the cut-open rat until 
the rat's liver had been placed in its mouth. This was ingested and 
the dog then immediately went over to the carcass and licked out 
the viscera. Excessive licking continued for over 4 min. Ths was 
followed by the dog repeatedly lifting up the carcass with the in- 
cisors; the forelimbs were not used to secure the carcass beneath 
the feet to facilitate dissection. This lack of coordination of 
forelimbs and teeth continued for approximately 6 min, when the 
dog lay down with the rat alternately between and under the 
forepaws as it indiscriminately chewed and mouthed the abdomen 
and appendages of the carcass. After 15 min, one forepaw was 
severed. Each time the pup pulled on the carcass, the latter would 
slip from under a forepaw. After 25 min, the head was removed 
and ingested. 

A third subject immediately grabbed and shook the carcass, 
gave several crush-bites, and attempted to bury it in one comer of 
the arena. This subject ate the rat's liver when given it ut su 
sequently ignored the carcass. The fourth subject also ate the Ever 

but ignored the carcass. , , . _ 

After the second prey-killing test, all four s"bl<=cts were mor 
reactive toward the carcass. The first subject bcked ou 
and inappropriately used the camassial teeth to ^ ,1,^ 

viscera. This took over 15 min. The normal reaction is to tear the 
viscera with the incisor teeth once the prey has 

the forefeet for counter-traction. This subjert never 

under the forefeet and subsequently ignored rat after ingesting 

the liver; it appeared incapable of dissecting t 

The second subject violently shook the ^ 

then appropriately (Lshed and severed the head 
sials and ingested it. The rest of the carcass was masticated ivith 



the camassials, the forelimbs now being better integrated with 
teeth actions, in that the subject would frequently hold the carcass 
under one paw while chewing the rat with the camassial teeth. 

Instead of using the incisor teeth and counter-traction with the 
forepaws to tear the skin, limbs, and viscera, the third subject 
continued to masticate the carcass with the camassials. Con- 
sequently, the carcass was not dissected or eaten. 

The fourth subject first used the camassials like the preceding 
subject, but after 6 min switched and used the incisor teeth in 
combination with forelimb counter-traction to tear and dissect the 
rat. The viscera were ingested followed by a long period of chew- 
ing the rat's appendages with the camassial teeth. This latter inef- 
fectual activity after 8 min was directed to the head of the carcass, 
which was cmshed, severed, and ingested. The remainder of the 
carcass was subsequently ingested. These observations are pre- 
sented in detail in order to demonstrate the role of experience in 
improving prey dissection and ingestion. 


The detailed ontogeny of prey-killing behavior in the coyote 
has been described earlier (Fox, 1969), and only the major points 
relevant to the present investigation will be presented (see Table 
11 ). 

In one Utter of four 8-week-old coyotes, all immediately 
grabbed and bit the rat, the bite being uninhibited. The coyotes 
immediately killed the rat and had dissected and eaten it within 1 
and 3 min, respectively. The other two killed their prey after 2.5 
and 5 min, respectively, each taking a further 2.5 and 7.5 min to 
dissect and eat the carcass. The slowest of these four subjects en- 
gaged in excessive bouts of head-shaking which was released 
every time the prey moved in the coyote's mouth. Long bouts of 
violent head-shaking continued during dissection of prey; when 
later retested, this same coyote engaged again in bouts of excessive 
head-shaking, but the bouts were less frequent than on the first 
test. All subjects when retested showed improved orientation of 
the grab-bite, striking the prey in the anterior thoracic region rather 
than aiming more posteriorly, which would give the rat sufficient 
freedom of movement to bite the subject's face. When retested all 
four subjects had killed and ingested the prey within 60 sec (aver- 

Effects of Domestication on Prey-Catching and Killing 


Table II. 

Coyote Female II, Group II (First Test) 

Immediate grab-bite-carry, then crush bite. Was bitten on 

1.5 min face— released rat, then grabbed around neck and thorax + 

violent head shakes. 

Multiple crush bites. 

2.5 min Crushes TW, AAV, TW, crush bites, AAV, TW. Crush bites, 

carries. AAV, TW, carries— intermittent play and crushing. 

4.5 min Pulverizing, holds with forepaw. 

Crushes head with camassials, holding body with one forepaw. 

7.5 min Eats off hind leg, then tail. 

11 min Eats off other hind leg. Uses camassials and forelegs well. 
Rips skin with incisors using forelimb counter-traction. 

33 min Eats intestines. 

24 min Uses camassials and removes and eats head. 

age 35 sec). None of these four coyotes played with the live or dead 
prey. All showed perfect coordinaHon of foreUmbs and teeth m 
pulling the carcass to pieces and used their teeth appropnalely 
the camassials to shear and crush and the inasors to puU and ear, 
in contrast to the beagles described earlier (that lacked fo^h^ 
coordination and used their teeth inappropnately, such as using 
the camassials to tear the skin and viscera). 

In a second Utter of six coyotes, the average killing tune w as 
3.3 min, all subjects immediately orienting and 
with no bite inhibition. Usually multiple cms . ‘ . 

terspersed head-shakes killed the rat. Two 

brief play-soliciting and tail-wagging, an a s , 

was inhibited. All subjects threw the rat across he arena wi h . 
powerful upwards and sideways head flick, the f' 

beine creater in the two subjects that engaged >n bnef bouts ol 

preceded by a vertical leap. Onl) one s J 
dead prey, even on retest. 


the dog: its domestication and behavior 

the camassials, the forellmbs now being better integrated with 
teeth actions, in that the subject would frequently hold the carcass 
under one paw while chewing the rat with the camassial teeth. 

Instead of using the incisor teeth and counter-traction with the 
forepaws to tear the skin, limbs, and viscera, the third subject 
continued to masticate the carcass with the camassials. Con- 
sequently, the carcass was not dissected or eaten. 

The fourth subject first used the camassials like the preceding 
subject, but after 6 min switched and used the incisor teeth in 
combination with forelimb counter-traction to tear and dissect the 
rat. The viscera were ingested followed by a long period of chew- 
ing the rat's appendages with the camassial teeth. This latter inef- 
fectual activity after 8 min was directed to the head of the carcass, 
which was cmshed, severed, and ingested. The remainder of the 
carcass was subsequently ingested. These observations are pre- 
sented in detail in order to demonstrate the role of experience in 
improving prey dissection and ingestion. 


The detailed ontogeny of prey-killing behavior in the coyote 
has been described earlier (Fox, 1969), and only the major points 
relevant to the present investigation will be presented (see Table 

In one litter of four 8-week-old coyotes, all immediately 
grabbed and bit the rat, the bite being uninhibited. The coyotes 
immediately killed the rat and had dissected and eaten it within 1 
and 3 min, respectively. The other two killed their prey after 2.5 
and 5 min, respectively, each taking a further 2.5 and 7.5 min to 
dissect and eat the carcass. The slowest of these four subjects en- 
gaged in excessive bouts of head-shaking which was released 
every time the prey moved in the coyote's mouth. Long bouts of 
violent head-shaking continued during dissection of prey; when 
later retested, this same coyote engaged again in bouts of excessive 
head-shaking, but the bouts were less frequent than on the first 
test. All subjects when retested showed improved orientation of 
the grab-bite, striking the prey in the anterior thoracic region rather 
than aiming more posteriorly, which would give the rat sufficient 
freedom of movement to bite the subject's face. When retested all 
four subjects had killed and ingested the prey within 60 sec (aver- 

Effects of Domestication on Prey-Catching and Killing 


Table III. 

Coydog, "Pale" Male (Retest) 

Immediate chase, grab-bite, cany, then investigates. Chases, 
carries, holds in paws, TW, bite intention, carries, mouths. 

5 min TW, nibbles (no blood). Play-soliciting posture, paws, nibbles, 

carries, weak head-shake. 

6 min Bite clearly inhibited; play-soliciting and TW combined with 

grab-bite, head flick and pawing and carrying. Bile becoming 
less inhibited. 

8 min Blood, mouthing, holds with forepaws, paws, frequent nibbles, 

paws, rat bites pup on Up — distress vocalization. Then more 
violent play, head flick, leap, grab and carry. 

9 min Holds with forepaws and begins to eat leg. Rat still alive. Now 

AAV, TW, play leaps, briefly, then chews and pulls forelimb, 

' holding rat down with forelimbs. Rat dying. 

13.5 min Now eating rat proper— eats head first. 

beagles, interaction with the prey was conHnuous (i.e., as m the 
coyote, motivation or arousal was more intense t an in e 
beagles). One subject in the first, and this same su jec an 
Others in the second test ingested dead prey (presen e wi 
abdomen cut open), all three animals showing per ect coor ' 
of head pulling and forelimb counter-traction to tear e pr ^ 
incisor and camassial teeth were used appropna e y o ^ ' ' 

and shear the carcass, and all subjects followe w a 1 ^ 

be the normal canid pattern of crushing, sevenng, and ingest g 

atole observations are summarized - Tabje IV which 
serves to illustrate the general trends of the three g p 
studied in this investigation. md 

In order to controWor the interaction Zs 

retest of prey-killing, where ■''f'" group of three 

presented with dead ,esied as follows: three 

6- week-old F, coyote x dog hybnds were lesic 

THE dog: rrs domestication and behavior 


When retested, all subjects spent less time chewing and sever- 
ing the appendages of the prey and assumed the normal sequence 
of crushing, severing, and ingesting the head, then crushing and 
tearing the rest of the carcass, pieces of which were ingested at 
random, usually the pelvic region and hind legs being ingested 
last; the caecum was rejected by two of the subjects.* 

F2 Coydogs 

All coyote x dog hybrids showed varying periods of play with 
prey, and all had clearly inhibited bites. Leaping and catching pat- 
terns were well coordinated and integrated, but the killing bite was 
absent. Most subjects toward the end of the first test, as in the 
beagles, developed more intense head-shaking, but in contrast to 
the beagles, the grab-bite-carry sequence was present at the begin- 
ning of the test. As with the coyotes, these hybrids never vocalized, 
while all beagles barked, yelped and growled at the live prey. 

The doglike leap and nose-stab was also seen in all six Fa 
hybrids. They would throw the live prey across the arena with a 
head flick and then leap upon it with a coyotelike high amplitude 
leap and forelimb stab. Only one of these subjects killed the rat 
after approximately 10 min, and, in fact, no killing-crushing bite 
was applied; the rat was essentially eaten alive, and on retest, this 
same occurrence was recorded. This clearly underlined the omis- 
sion or inhibition in the coydog hybrids of the killing bite, although 
all other prey-catching patterns were evident (see Table III). 

As the tendency to shake the live prey increased toward the 
end of each test and was much more frequent in the second test, so 
the inhibited bite and multiple nibble-bites became more intense. 
In the second test, only one other coydog killed the prey after 8 
min, and the multiple killing bites (combined with violent head- 
shakes) appeared to be disinhibited nibble-bites. This subject sub- 
sequently ignored the dead prey. The frequency and duration of 
play bouts were less in all subjects in the second test, yet unlike the 

Ejfects of Domestication on Preif-Catching and Killing 


Table V. 


Response latencies 
of subjects (sec) 


Actions patterns 










































®Ate dead, dissected prey at end of test. 
‘’Partially killed and ate live prey. 

was inhibited in all trials and no head-shakes were recorded, al- 
though the actions of grab-bite and cany, stalking, leaping, an 
play-soliciting were recorded. Occasional head-shake 
while approaching the rat were recorded in this subject in na s 
and in. The subject handled dead dissected prey in an uncoordi- 
nated manner resen ibUng that of the beagle, and the general 
phenotypic features of this Fz hybrid \vere closer to beag ^ 
coyote. S„ which phenotypically resembled rnore 'he 
its prey on the thiJd trial after 8 min; the head-shake first appeamd 

in this trial after a long latency, and as observed in e o ? • ■ 

group, there was a^dual disinhibition of 

nibble-bites increasing in intensity until the Pr ^ 

around the thorax. This subject, as also obser^'cd in the f g ^p 

of hybrids, began eating the prey while it was ® ‘ ‘ 

and S 3 showed good coordination of ‘ stronc head- 

gesting dead prey. Throughout all trials Ss shou 


THE dog: its domestication and behavior 

Table IV. 

normal temporal sequence of prey-catching and killing 
in coyote 

(With point of truncation ofsequencein beagles o/Fg coyote x dog hybrids) 

Orientation ►approach ►investigate ► play 

grab-bite (with or without leap 
and forelimb stab) 



2 *>.. 

crush (kill) bites 
- and head shakes 



“1, Level of truncation of temporal sequence in all four beagles, first test. 

Level of truncation of temporal sequence in all four beagles, second test. 

'3, Level of truncation of temporal sequence in all F* coydogs, first test, the kill-bite 
being inhibited in four out of six subjects. 

'‘Complete follow-through of temporal sequence occurred in only one coydog, and in 
this subject there was no clear kill-bite. 

consecutive days of testing, each test lasting lo min, and dead 
dissected prey being given not after the first trial as in earlier 
studies, but after the second trial day. In this way, the contribution 
of experience with live prey in Trial I influencing performances on 
Trial U could be separated from the possible added effects of ex- 
perience with dead prey between Trials I and II. 

The data are summarized in Table V. An overall decrease in 
response latency over successive trials is evident. In Si, the bite 

Effects of Domestication on Prey-Catching and Killing 


one individual in the second litter killed the rat after 10 min; multi- 
ple nibble-bites to the body became disinhibited and suddenly the 
thorax of the prey was crushed. The rat was then eaten. Although 
the prior group test in the arena with prey did not reveal any social 
facilitation of prey-killing, social facilitation (i.e., competition) may 
have triggered prey-killing in the home pen, as emphasized by 
Leyhausen (1973) in his studies of prey-kiUing in cats. The signifi- 
cance of a particular place to eat and hunt is worth further investi- 
gation. Burrows (1968), for example, records that red foxes may not 
kill prey within their denning area, and a rabbit or ground-nesting 
duck may even share the same denning site. The same animals 
would undoubtedly be killed if found in the fox's range when it 
was out hunting. 


In the four beagles tested, all subjects interacted with the prey mov- 
ing under the sheet. However, the interactions were of very brief 
duration, and all four subjects never exhibited either vertical leaps 
or forelimb stabs. The quantitative results of all tests are reported in 
Table VI. In most trials the beagles spent a great deal of time in 
both play-soliciting and self-play behavior. Frequently a subject 
would completely ignore the prey for most of the test and then 
finally spend a minute or two growling, barking, and nibbling at 
the prey. All subjects would claw with their forepaws at the prey 
when the prey was lying immobile against the side of the observa- 
tion arena. When the prey attempted to escape from the beagle, the 
subject's most intense response would be a nose-stab, whereas the 
other two species would respond with a forelimb stab or a vertical 
leap and stab. There was no significant difference found to exist 
between Trials i and 2 for the beagles' scores for forelimb stabs and 
forelimb stabs with vertical leap. 

In contrast to the beagles, the three coyotes tested showed 
high frequencies of both action patterns and on the whole the 
coyotes spent significantly more time interacting with the prey. The 
coyotes followed every mov'ement of the prey; they would stalk 


THE dog: its domestication and behavior 

shake action, but the bite was inhibited and all prey were unin- 
jured at the end ol each trial. Clearly, the experience with dead 
prey between Trials II and III had no appreciable effect on the 
prey-killing tendencies of Si and S3. Such experience may have 
contributed to the development of crush-bites which almost killed 
the prey of S3, but another interpretation can be offered, namely, 
the increasing arousal, short response latencies and increasing du- 
ration of interaction over successive trials and the close temporal 
linking between head-shaking and crush-bites in this subject. Fur- 
ther studies are needed in order to determine the relative impor- 
tance of maturation, increments of experience with live prey, and 
the effects of ingesting dead prey on the development of preda- 
torial action sequences. 

F3 Coydogs 

None of the eight F3 generation coyote x dog hybrids from 
three litters killed prey on the first test, and when retested, only 
one killed and ingested its prey. With this one exception, all sub- 
jects showed only brief interest in prey during the first test, reac- 
tions being orientation and following but no contact. When re- 
tested, additional reactions appeared, grab and carry in two sub- 
jects and head-shake and bite intentions in another. Reactions in 
the third trial were virtually the same. The one F3 hybrid that killed 
after a latency of 6.5 min on the second test was the most respon- 
sive in the first test. It immediately grabbed and then carried the 
live prey and after 7.5 min gave a mild head-shake. After this it 
continued to play intermittently with the prey until the end of the 
test period. 

Clearly, the F3 hybrids have a significant repression of prey- 
catching and killing behavior. This could be because they were 
more disturbed than the other canids when in a relatively unfamil- 
iar place (i.e., the testing arena). In order to assess this possibility, 
they were tested again in their home cages. (The day prior to this, 
each litter of three pups was placed together in the arena with live 
prey. It was virtually ignored, subjects engaging in social play in- 
stead.) In each litter a tug of ivar began over the dead prey placed 
in their cage. It was not eaten, however, and was treated like a play 
object. With live prey, one litter did not kill in its home pen, while 

Effects of Domestication on Prey-Catching and Killing 


and chase the rats, trap them, and make uninhibited bites, head- 
shakes, and several forelimb stabs and leaps. One coyote actually 
killed the prey. In the two tests, the prey was killed with a crush- 
bite, and then the coyote attempted to pull the dead rats through 
the sheet. In three other subsequent retests, the prey were appar- 
ently the victims of the forelimb stab with vertical leap. In these 
cases, the subject ignored the rats after they were killed. 

Among the F, generation beagle x coyote hybrids, there was a 
high frequency of both forelimb stabs and vertical leaps, and the 
total interaction time between subjects and prey was higher than in 
both the beagles and coyotes. (See Table VI.) All of the hybrids 
required approximately 2-5 min to adapt to the observation arena. 
In contrast, the beagles sometimes spent the first 10 min adapting. 
This adaptation period consisted of the following types of be- 
havior: initial investigation of the arena (ignoring the prey), several 
attempts to escape from the arena, self-play (tad-chasing and 
jumping in the air), and finally encounter with the prey, usually by 
accident. Once the Fj hybrids did encounter the prey they became 
highly aroused. Most subjects exhibited a high frequency of 
forelimb stabs. These were usually elicited by small movements of 
the prey. In contrast to the coyotes, the beagle x coyote hybrids 
never used a crush-bite on the prey (emphasizing this same point 
observed in the previous test with live, visible prey). All the hy- 
brids' oral contact with the prey consisted of either inhibited biting 
or multiple inhibited itibble-bites. As in the case of the coyotes, the 
coydogs exhibited a high degree of arousal and motivation as evi- 
denced by the high frequencies of forelimb stabs and leap-stabs, 
long bouts of intense stalking behavior, and long periods of in- 
teraction time with the prey. The hybrids also displayed a high 
incidence of what may be referred to as place memory. For exam- 
ple, the subject would be interacting with one of the two prey, then 
would move to the other rat some distance away and then, after 
some time, suddenly turn and make a high ampUtude vertical leap 
directly at the spot where the first prey had been located. Many of 
the leap-stabs were observed in this context or when one of the 
hybrids was chasing a fast escaping prey. In the latter case, the 
subject would make one or two fotelimb stabs at the prey; the prey 
would then start to flee, at which point the subject would make a 
vertical leap and stab. 

r.iWf VI. 


THE dog: its domestication and behavior 

Effects of Domestication on Prey-Catching and Killing 


The motivational state may therefore change with experience 
and may vary between individuals and between species and hy- 
brids; differences in conflicting motivations, such as the tendency to 
play or to be fearful of the test situation as emphasized by Mason 
(1967), must also be considered. 

It may be postulated, therefore, that optimal arousal and 
motivational conditions are essential for the release of certain ac- 
tions before experience per se can have any effect upon them. 

The inferior prey-killing ability in beagles and in some of the 
coyote X dog hybrids may be due to a delaying effect (of domestica- 
tion) in the maturation of this behavior. Thus, it may be argued 
that the age of 8 weeks may be too early to test prey-killing in 
beagles and certain hybrids. Such animals when retested at 10 and 
12 weeks of age did not, however, show any further improvement 
in prey-killing ability, and it is unlikely, therefore, that there is any 
delay in maturation per se, but rather, as implied from this study, 
there is a change in threshold and truncation of the temporal or- 
ganization and sequencing of action patterns attributable to domes- 

Analysis of the two action patterns, forelimb stab and leap- 
stab, reveals that these actions are a predominant part of the be- 
havioral repertoire of the coyote and coydog hybrid, but under the 
test conditions (concealed prey) they were not reported in the 
beagles. This apparent absence in the beagles may be correlated 
with their low overall duration of interaction scores, which indi- 
cates that they were less aroused than the coyotes and hybrids. The 
fact that in one beagle leap-stabs were occasionally recorded when 
retested with live visible prey supports the arousal hypothesis al- 
luded to earlier in this discussion. A second possibility is that the 
forelimb stab and leap-stab occur at a lower frequency in the 
beagles because they have a higher threshold; a greater degree of 
arousal is needed for its release than in the coyotes and hybrids. 

Bite inhibition was clearly manifest in the beagles and their 
coyote hybrids, and inhibition could not be attributed to moti- 
vational factors alone since the hybrids were highly motivated 
even though they showed bite inhibition. This notion is supported 
by comparative developmental studies of early contactual and ag- 
gressive behaviors in coyotes, wolves, dogs, and wolf X dog hy- 
brids (M. W. Fox, personal observations) and prey-killing abilities 


THE dog: its domestication and behavior 


The two related studies bring out a number of intriguing points, 
the genetics of which can only be speculated upon at this stage in 
view of the small sample of coyotes, beagles, and hybrids used in 
this project. More precise genetic inferences may be drawn in fu- 
ture studies involving not only a larger n but also Fj and back-cross 
coyote X dog hybrids. In spite of these limitations, qualitative and 
quantitative differences in prey-catching and prey-killing were re- 
markably consistent within groups arid add to our understanding 
of the effects of domestication on canid behavior. 

The most striking and consistent findings were the absence of 
bile inhibition in the coyotes in the two tests where the prey was 
either visible or visually concealed and complete inhibition of the 
prey-killing bite in the beagles. In contrast to these extremes, two 
of the Fj hybrids showed a gradual release from inhibition, and 
although prey were eaten, they were not as effectively killed as by 
the coyotes. 

The difference in the degree of bite inhibition may account for 
the truncation of temporal sequences of prey-catching and killing, 
but it should be remembered since temporal organization is varied 
during play, that coyotes will play vrith live prey for variable 
periods and at such times show clear bite inhibition prior to killing 
the prey (Fox, 1969). The truncation of the sequence may be at- 
tributable to differences in arousal in the beagles and hybrids com- 
pared to the coyotes, a high degree of arousal being necessary for 
actions such as crush-(or kill) bite, head-shake, forelimb stab and 
leap-stab to be elidted. 

Another related hypothesis is that the action patterns as- 
sodated with prey-catching and killing are ordered temporally on 
the basis of threshold differences, those actions toward the end of 
the sequence having a higher threshold than earlier actions. A 
minimally aroused subject would then only show low threshold 
responses such as orientation, approach, and follow, as was the 
predominant feature of the beagles in the first test. Arousal (or 
motivation) may therefore increase with experience with prey, so 
that higher threshold action patterns are incorporated appro- 
priately into the temporal sequence. This hypothesis is supported 
by the retest data from beagles with visible prey. 

Effects of Domestication on Prey-Catching and Killing 


Table VII. 

Complete hunting sequence of 
wild canid 

Tracking, trailing 

Herding, driving 

Stalking, pointing 

Attacking, killing 

(for cubs/mate) 

Partial sequence of some 
domesticated dogs^ 

Bloodhound, gazehound 

Sheep dog 

Setter, pointer 



■Attack inhibited in most breeds. 

average kill latency of 15.5 min. When retested, this latency drop- 
ped to 10.5 min. Interestingly, one pup, prior to killing, held the 
prey with its forepaws and pulled at its legs and tail, the consum- 
matory (eating) phase occurring before the killing bite. 

This clearly demonstrates that inheritance does influence bite 
inhibition — a point of considerable social significance in view of the 
number of people being bitten by dogs today (estimated 400,000 
per year in the United States). While improper human handUng 
may often be to blame and/or inadequate socialization (Fox, 1972), a 
relaxarion of selection for stable temperament and bite inhibition 
may also be involved especiaUy in those breeds that become popu- 
lar and are mass-produced, with Uttle quality control, to meet pubUc 
demand. The release from inhibition in well-socialized dogs for 
attack training can be effected by increasing arousal through play- 
fighting with a padded sleeve. A gradual disinhibition occurs 
without disruption of the social bond. This unlearning of a socially 
inhibited response (biting) is analogous to the gradual appearance 
of the killing bite in coydogs where motivational factors or social 
inhibition per se may be involved. The reaction of beagles toward 
live prey was essentially one of social play and logically, social 
inhibirion of biting occurred. This conclusion was also made m 
earlier studies of prey-kilUng behavior m wolf cubs. Those that did 


THE dog: its domestication and behavior 

(Fox, 1969). Around 24-30 days of age, contact with a conspecific 
frequently releases an uninhibited bite in coyotes (and also in 
young red foxes of this age), and it is only after dominant- 
subordinate relationships have been established that the bite be- 
comes inhibited. Prior to this time, play behavior is rarely seen. In 
contrast, wolves and dogs show marked intraspecific bite inhibi- 
tion and also inhibition of prey-killing bite, which in part accounts 
for the fact that they engage in sustained bouts of contactual and 
play behaviors compared to coyotes and foxes (Fox, 1975). The 
conclusion, then, is that there is a greater degree of genetic control 
of bite intensity in domestic dogs (beagles), while in coyotes selec- 
tive control is effected more through social and experiential influ- 

In some breeds of domesticated dogs, notably in the bird dog 
pointers and retrievers, there has been rigorous artificial selection 
for "soft mouth," for the dog must not mark the game. The prey- 
catching sequence in such breeds consists of orientation, approach 
(or track), and either point or grab and carry (retrieve), the killing 
bite and head-shake actions being selechvely eliminated. 

Vauk (1953) reports that play with prey (and vrith inanimate 
objects) develops at different ages in different breeds of dog. He 
concludes that domestication has modified or completely inhibited 
prey-killing, in certain breeds; some, like the pointer, develop 
fixed, exaggerated signs. The effects of selective breeding and 
training on prey-catching and killing behavior in the domestic dog 
is summarized in Table Vn. It is evident that domestication and 
selective breeding may lead to a breakdown in the normal temporal 
sequence at one of several points by intensifying or inhibiting cer- 
tain action patterns. Various breeds, selected for specific hunting 
and tracking tasks, clearly demonstrate this subtle aspect of domes- 
tication. The capacity of domestic dogs to hunt and kill prey and 
live independently has been demonstrated in feral dog studies (see 
Chapter 3). Therefore, these abilities are not eliminated through 
domestication, but rather, motivation, threshold of different ac- 
tions, sodalization, training, and dependence upon man are some 
of the interrelated variables that must be considered in evaluating 
the effects of domestication upon animal (and human) behavior. 

Two 8-weck-old Australian dingos (undomesticated) were re- 
cently tested. All lolled and ingested prey on the first test, with an 

Effects of Domestication on Prey-Catching and Killing 


are highly innervated in carnivores to provide tactile feedback so 
that the positioning and pressure of the bite can be exactly con- 


In order to identify possible effects of domestication on behavior, 
prey-catching and killing behavior was studied in domestic dogs 
(beagles), coyotes, and Fj and F3 generation beagle X coyote hy- 
brids. The full temporal sequence of prey-catching and killing, to- 
gether with efficient dissection and ingestion of the prey evident in 
coyotes at 8 weeks of age, were respectively truncated and disor- 
ganized in the domestic dog and hybrids. These changes in be- 
havioral organization and temporal sequencing of action patterns 
are discussed in relation to differences in arousal (motivation) and 
response threshold. Partial and complete inhibition of the killing 
bite was found in hybrids and beagles, respectively, this being a 
major factor in the truncation of the full prey-catching and killing 
sequence. Domestication may lead to truncation of this temporal 
sequence at one of many points by intensifying or inhibiting certain 
action patterns through selective breeding. 


THE dog: its domestication and behavior 

not kill live prey showed playful and actively submissive actions 
toward the prey, but after being forcibly fed dissected prey, they 
essentially learned that it was food and from then on would attack 
and kill prey and direct no further social behavior toward it. 

Thus, some species (wolves) have to learn what to kill and 
what is food, while in others (foxes and coyotes) learning has less 
influence (Fox, 1969). The argument here is that there may be some 
connection between intraspecific aggression, general bite inhibi- 
tion, and prey-kilhng. By analogy also there may be considerable 
resistance and conflict in training a dog to selectively attack certain 
people (on command or without command in a certain place they 
may ^ard) and not to attack other people or in other places, when 
there is socialized attachment to people and generalized bite inhibi- 
tion. Therefore, no single factor is wholly responsible for prey- 
killmg and social inhibition of biting in wolves or of selective disinhi- 
ition of attacking and biting man in trained guard dogs. Genes, 
early experience, social attachment, and training all contribute to 
^ expression of these motivationally separate activities of 

I^ey-killing and agonistic behavior. Social attachment to prey 
(Kuo, i960) may inhibit prey-killing behavior; intraspecific bite in- 
associated with a more generalized bite inhibition 
w ich has to be disinhibited in relation to prey in some species 
sue as the wolf. Thus, although motivationally distinct, certain 
vanables may affect both aggressive behavior and prey-killing reac- 
tions equally or in a similar direction; hence perhaps the frequent 
hatior'^”*^^^^ association between hunting and aggressive be- 

Similarly, wolf cubs show more social inhibition of aggression 
and ^ting conspecifics than coyotes and foxes who at an early age 
may a conspecific reflexively as though its fur and movement 
re eased a prey-killing response. Social experience in controlling 
Dite inhibition in coyotes and foxes is therefore important in early 
lire, while release from a more generalized inhibition of biting is 
necessary for some wolf cubs to secure live prey. 

In future studies it would be advantageous to use pressure 
transducers to provide quantitative data on developmental 
changes and on spedes and breed differences in bite intensity and 
control. The contribution of genetic and experiential influences 
might then be eluddaled. Ewer (1973) notes that the canine teeth 


Interaction Differences 
in Play Actions in 


Most studies of social behavior have focused upon intraspecies 
interactions. This study involves a little explored area of in- 
terspecies social interactions, where the frequency of occurrence of 
clearly identified discrete action patterns may be modified in rela- 
tion to the degree of dyadic compatibility within the selected con- 

text of playful interaction. . , , 

Yves Rouget (personal communication) raised a red fox (yulpes 
vulpes) with a domesticated dog. The impressive, but unquantified, 
consequence which he recorded on film was the high frequency of 
face-oriented pawing manifest by the fox. Such an action is rare in 
foxes but is a common action pattern in domesticated dogs. This 
kind of observation opens the question of the role of expenence m 
the development and reinforcement of species-typical achon pat- 

An incompatibility of reciprocal actions has been reported by 
Blauvelt (1964) between sheep and goats raised together, no effec- 
tive fights were seen because the sheep tried to butt the goat and 
the goat tried to jump on the sheep. Interestingly, whom the am 


Interspecies Interaction Differences in Play Actions 


lowed by side-to-side head flexions which move fluidly down the 
body, followed by rolling over, "spinning," running around the 
partner, "diving" or exaggerated approach or withdrawal (Fox, 
1971b). From the play-soliciting bow, the head may be twisted up- 
ward toward the forelegs, throat, or cheeks of the congener and 
bite intention lunges or incomplete bites are then executed (Figure 

An action resembling the play-leap occurs when one coyote is 
chasing another; the action is of Jow amplitude and is followed by a 
bite or bite intention on the rump or shoulders of the partner or by 
a forelimb clasp (Figure 1). This clasp, which is often never fully 
executed, consists of seizing the partner around the waist and fre- 
quently following with a scruff-oriented bite. The partner may 

Figure 2. Although scruff-oriented biting in coyote (D) nffen oc- 
curs during play-fighting, the coyote usually approaches low (A 
and B) and makes an upward directed bite from the <C) play- 
soliciting posture and rarely directs vertical leaps at its partner. 



mal attacked was determined by early sodal experience, but the 
manner in which it attacked remained unchanged. 

A consistent feature of social play in C. familiaris, Fi C. familiaris 
X C. lupus, and FjC. familiaris x C. latrans is the occurrence of the 
play-leap (Figure i). This action may be preceded by a direct stare, 
a play-soliciting bow or an incomplete leap intention which may be 
repeated three or four times. The leap itself varies in amplitude and 
may be repeated as the subject moves in on its congener. The latter 
may also rear up and meet its partner with a reciprocal leap, and 
both animals briefly stand and wrestle with the forelimbs and make 
face-, cheek- and scruff-oriented bites or incomplete bites. Most 
often the leap is followed by an incomplete bite or bite intention or 
by a nose-stab which may be interpreted as a bite intention move- 
ment. Occasionally this may be followed by a backward leap. 

In the coyote, C. latrans, such sequences involving the play- 
leap are not observed. In this species, a play-soliciting bow is fol- 

Figure i. (A) Vertical leap of beagle during play which may be re- 
ciprocated (B) and both rear up. Leap may be followed by face- or 
cheek-oriented bite. (D) Playful standing cater by F, coyote x beagle; 
<E) clasping by coyote during play-fighting. 

Interspecies Interaction Differences in Play Actions 


Table I. 



With beagle 

With coyote 

With coydog 


8.5“ (2-16)'’ 

16.3 (1-37) 

15.7 (2-35) 


1.0 (0-2) 

2.5 (0-7) 

0 (0) 


12.7 (1-31) 

5.7 (4-9) 

16.0 (7-22) 

“Average scores per individual. 
•"Range shown in parentheses. 

coydog than with its own species and this may account for the 
lower scores in beagle pairs. , , . , 

An intriguing finding was that the coydogs had high frequen- 
cies of play-leaps when paired with a conspeafic or beagle but 
lower frequencies when with the coyote. This was attributed not to 
a lowered activity or motivation, for play was intense, ® 

possibility that the hybrids had a more fleidble or adaphve play 
repertoire which could be reciprocaUy matched with a beagle or 
coyote partner. In contrast, the beagle when paire 
showed the highest average frequencies of P ^7' were 

not reciprocatel No significant differences attnbutable to sex were 

evident in any of the three canid types. 


These data support the are bi'com 

quences of beagle and coyote ^unng intentions of 

The bow followed by upward direc play-attack; the play- 

the coyote may be regarded as Im ^ P piay.atiack 

leaps of the beagle may be attack orientation. 

The coyote, in responding to j or hip-slam to block or 

twists away and usually executes a K-agle but 

deflect the attack; such actions were nrobablvcontnbuted to 

were evident in the coyote x dogs and most prob . 


THE dog; rrs domestication and behavior 

attempt to avoid being clasped by executing a hip-slam or twisting 
around to face its congener. When facing, rearing up may occur, 
followed by face-oriented bites or bite intentions and pushing with 
the forelimbs. 

Materials and 

With these species-characteristic actions in mind, it was decided to 
evaluate the compatibility and reciprocity of such action sequences 
in variously combined pairs of subjects, by recording the frequen- 
cies of play-leaps. All dyads were of opposite sex, each approxi- 
mately 12 months of age. Each pair (of noncage mates) was ob- 
served for 10 min play in an 8 x 8 ft soundproofed arena equipped 
with one-way observation windows. Two observers recorded the 
frequency of play-leaps for each pair, dyad combinations consist- 
ing of beagle X beagle, beagle x coyote, beagle X coydog, coyote X 
coyote, coyote x coydog, and coydog X coydog. A total of 20 dyad 
combinations were tested in 12 subjects (4 beagles, 4 coyotes, 4 
coydogs, with 2 females and 2 males per species). 


The findings are summarized in Table I. It should be noted that 
both coyote and coydog showed hip-slams during play, but the 
frequency of this action was not recorded. Also, several of the low 
amplitude play-leaps recorded in the coyote were difficult to dis- 
tinguish from the incomplete action of rearing up to clasp the part- 
ner with the forelimbs. 

The high frequencies of play-leaps in pairs of beagles, pairs of 
coydogs, and beagle X coydog reflect the reciprocal nature of this 
action. In all dyads where one individual scored over 15 play-leaps, 
then its partner likewise had a comparably high score. 

The beagles were more active when paired with a coyote or 

Irtferspecies Interaction Differences in Play Actions 



Spedes-typical patterns were identified in wild and domesticated 
canids during play in dyads of the same or different species. While 
these actions are under relatively rigid genetic control (i.e., are 
inherited) other dimensions of the jjlay sequence may be more eas- 
ily modified contextually. Thus, not only species and context de- 
termine the frequency of occurrence of certain actions but also the 
compatibility of the interactee, be it of the same or of a different 
species. The long-term consequences of interspecies interactions 
under conditions of captivity may lead to more permanent changes 
in the occurrence, frequency, and amplitude of certain species- 
typical, ''fixed" action patterns. This may be an additional variable 
to consider in investigating the complex influences of domestication 
upon behavior and warrants further investigation. 



their ability to maintain reciprocal synchrony with the coyotes dur- 
ing play bouts. These hybrids also showed the play-leap action 
which enabled them to sustain reciprocal play actions with the 

■pie role of early experience and of social factors should also be 
considered, and this point is emphasized here rather than earlier in 
this book, with reference to the prior experiences of our canids. 
The criticism that might be leveled at this study to the effect that 
the beagles had no prior opportunity to interact and modify their 
achons with respect to coyotes (and vice versa) is untenable. All 
beagles and coyotes used in this study had been reared together 
from approMmately 8 weeks of age, although tests were conducted 
using indmduals from different cages. It might be expected that 
coyotes with such early social experience might acquire the play- 
leap achon of the beagle. But this was not evident; thus supporting 
the nohon that the play actions studied are species-characteristic 
mav h/ Tfi frequency and temporal sequencing of which 
may be modified contextuaUy as in certain dyadic interactions, 
the interaction with a different species may modify 

oi^nH of certain action patterns, more pro- 

long-lashng effects on interspecies interactions under 
evahiateH* ^®.“®‘“"®^®nforced contact in captivity remain to be 

" "t’ '"‘i^nge in the structure 
anH fr occurrence 

? elicitation may be altered, especially within the 

and dncr u ’^"^^J^^cation, as when different species (cat 

and n d ; I’”ses, etc.) are raised 

on tnrh H ® influence of human behavior 

canid evaluated. One classic example is the 

canid analogue of the human “gieeKng grin" (which is quite dis- 

(Fox iQ'^W ™ssive grin and open mouth play-face of canids 
onw'h®^^ ®’‘P''®“i°n is mimicked by the dog and has 

anLorn^’''" interactions and not between dog 

famar d^' " ^'®°.^''nience that the capacity to elaborate this 

dPvtln^ iines of dogs will never 

ITp wL 1 I “Pi*® others from the 

dov I -i*^ parents have this facial expression will quickly 

develop It either spontaneously or with a little human reinforce- 


Socialization Patterns 
in Hand-Reared Wild 
And Domesticated 


This chapter offers a number of observaHons about expenences 
with hand-raised and socialized canids, including wo ves, coj^ es, 
golden jackals, and red foxes. When assembled, these ^necdo es 
constitute a long-term experiment on these caP'.v. t , 
where their social reacHons toward peopl^an be contrasted .. 
their natural or innate social tendencies. The 
long to three basic social types (Fox, 1975); (covotc 

(red fox), transitional Type II with 

and golden jackal), and the social Type t mnsiclhtion 

legiaLs and pack formation (wolO- 

of primarily inLrited tendencies, -'h expenen .a ac 

tors during early life, is a ■^njordeterm.nan of sckuI Khm .or an^^^ 

of the capacity "to form --nta.n s-al r« 
life. In this chapter, it will bo shown how the in 
of social ->.-.>ionships in the^ thre^ 
reactions toward people aiter inej 
dalized to human beings. 

Socialization Patterns in Wild and Domesticated Canids 


patterns of human contact in no way resembled the aforemen- 
tioned restricted rearing and socializing conditions. 

The distinctions made by Scott (1968b) between primary and 
secondary socialization should be emphasized here. Primary so- 
cialization refers to those social relationships which are established 
early in life during a critical period (Scott 196^) between a wolf 
cub, its parents, and littermates. Secondary socialization refers to 
those social relationships that develop at a later age, as between 
other adults of the pack that breaks up during the denning season. 
The possibility that species differ in their capacity to establish and 
maintain secondary social relationships will be explored in this 


Primary social bonds may facilitate secondary socialization; a 
domesticated dog, for example, if raised with human beings early 
in life is able to generalize from these primary socializing experi- 
ences and is friendly toward strangers at a later age. Some breeds, 
notably the guard dog types, seem to have a more limited capacity 
to form secondary social relaHonships and are very wary of stran- 
gers, The relationship between this phenomenon and the compara- 
ble behavior in the wolf will be discussed subsequently. 

Woolpy and Ginsburg (1967). in their extensive sl^ies of wolf 

socialization, have shown that adult wolves caug t vvi , wi car 

ful handUng, wiU become socialized to their handler and on the 
basis of such experience tend to generalize 

strange people as well. These findings put a different light on the 
critical period hypothesis but in no way refute it. ins .“^6 '''^P 
that coyotes do not generalize or form 'miin 

ships to the same extent as wolves, ""f 'V";;;;';," 

attached to the principal person responsible S P 

socialization. This is the key to the present report; 
extent do the socialization capacities and ‘ 

beings of captive canids match their natural 
ecologically adaptive, genetically determine soci. p, 


For convenience, the results are broken " 

tions, and each section is discussed separateir The se-ctu n. 


THE dog: its domestication and behavior 

Materials and 

The following observations are based on experiences with is wild 
canids, all hand-raised from 2-6 days of age and kept in captivity 
under similar conditions of handling and management until sexual 
maturity (2 years) and in some animals up to 4 years of age. Sub- 
jects include i male and 2 female wolves, 2 male jackals, 2 female 
and 1 male red fox, and 5 female and 2 male coyotes. In addition, 6 
beagles, 8 pointers, and 4 Chihuahuas were raised under similar 
conditions for comparative purposes. 

theoretical premise 

reactions of these animals, all with 

anZnw^ Iiand-reared them, 

and toward research assistants who later took care of them. Over a 

son who almost daily contact with the per- 

son who had raised them and also regular contacts with an average 

siHriTr^ ‘w°/e‘r'ale assistants per week, who were respon- 

was aoor f ^ ^ate of persomel 

o^^ ^ “ months. The social conditions in 

of human contact were therefore 
studW h" " ‘l^at those students 

S fn nontraumatic contact in- 

viiums werr?®" P^r year. Occasional 

Tn summf i“”'" 1 faciUty on a random basis, 

ma r^xT ^nntact/Lposure to approxi- 
mate whethiR^"°‘’f ^ach year. It is imposSble to 

sociali^tnot '""‘act facilitates Lcondary 

soda cotftm, the annual turnover eventuaUy leads to 

H experience with such 

nt^sr *at most dogs readily accept 

one ort!? ■ ^ Coyotes raised exclusively by 

ZZIT. ’’'Tk "“'=P‘ a ehange in personnel or 

change of sex of handler and will show fear or aggression toward 
the new person (personal observations). In the priient chapter the 

Socialization Patterns in Wild and Domesticated Canids 


arbitrarily categorized as follows: permanence of primary social 
attachments, capacity to form secondary or subsequent attach- 
ments, changes with sexual maturity, socio-sexual discriminations. 
In each section, the behavior of the canids toward human beings is 
compared and contrasted with their intraspecific behavior in both 
captivity and in the wild. (See also Table 1.) 


All subjects, irrespective of species and sex, remained attached to 
the author who hand-reared them. They all showed active submis- 
sive greeting and passive submission when physical contact was 
made. The red fox, however, tended to avoid physical contact in 
spite of showing active submissive greeting and occasional play 
solicitation. When contact was forced, the fox would remain pas- 
sive or attempt to escape and occasionally bite. The active greeting 
by this species involved virtually no physical contact in contrast to 
the face-oriented licking, pawing, and jumping up of the other 
canid types. In the wolves, actual contact initiated by the anirnal, 
including rubbing and contactual leaning, was of greater duration 
than in the Type II canids (coyote and jackal). 

It may be concluded that in these three canid types, proximity 
tolerance was lowest in the red fox (Type I), while maintenance of 
close proximity was greatest in the wolf (Type III). The coyotes an 
jackals (Type II) were essentially intermediate; in the coyo'es. 
greater individual variation in proximity tolerance devc ope wi 
increasing age. Some individuals after 2 years of age i\ou on > 
briefly greet, and then withdraw, while at an ear ler age uou 
maintain contact and display active and passwe su mi^ion or a 
longer period. Others did not show such a change '' ' _ 

offensive or defensive aggression W.1S ever disp a> e ) , 

and III canids toward the author, while such occurrences were not 
infrequent in the Type I canid. In ‘'vo instances the author as 
subjected to redirected aggression during a con ic ' 
coyotes; one of the pair redirected its attack on the hnneher. . u 
bites being inhibited, hmvever. No "penences Im c ^emred 
with the wolves. All domesticated hand-raise months of 

tached through to maturity, some individuals after 5 

Table 1. 


Socialization Patterns in Wild and Domesticated Canids 

have hand-raised wolves. What evokes fear of men — odor (andro- 
gen metabolites) or human male body langage— remains to be 
evaluated. With sexual maturity (2 years) this wolf also showed 
increasing aggression toward conspedfic females (and also female 
domesticated dogs) but displayed active and passive submission 
toward male wolves and large male dogs. These reactions were 
more intense during estrus in February. 

Of the two male jackals^ one was more timid and would only 
greet and maintain proximity with the author; fear of strangers was 
evident before 1 month of age in this animal. The other jackal 
remained friendly toward strangers until approximately i year of 
age. Increasing ambivalence between approaching, greeting, in- 
vestigating, and solidting grooming and withdrawing was evident. 
Subsequently, this animal began to threaten strangers in a highly 
ambivalent defensive-offensive display, showing more offensive 
aggression toward men than women. By 2 years of age, he ha 
attacked and sUghtly injured two females who were regular atten- 
dants and one strange female; strange males could not even enter 
the cage. 

The seven coyotes were similarly friendly toward strangers, 
new, and regular personnel irrespective of sex until after 1 year o 
age. After this age, aU animals began to show increasing hesitation 
to approach, creet, and investigate strangers, with only one excep 
Hon. This animal, a female, instead showed increasing aggression 
toward males and occasionally toward females. One ma ' 

females of the remaining six coyotes became increasing y ‘ 
and would remain in their nest boxes when either regu ar pc 
nel or strangers came close. The remaining I ree 
indifferent, in that they would not greet strangers or gu pc 

sonnel, but they did not show "ge provides an 

Another male coyote, obtained at 2 
additional example. This animal had been L 

women and remained attached to them as f,._ni«and was 

years of age he was kept and mistreated by a This covote 

<,ve,l»,lly gl... ,0 Ih, mn-pl”" 


THE dog: its domestication and behavior 

age showing a tendency toward passive submission rather than 
active submission (friendly greeting) when handled by the author. 
This correlated with a tendency toward avoidance (fear) of strang- 
ers in such dogs, but after brief exposure, unlike the wild canids, 
they would become more active and begin to accept strangers. This 
capacity for secondary socialization (or social potential per se) con- 
trasts the more limited capacity evident in nondomesticated canids 
(see below). 


Between 1 and iVr years of age, the wolves began to show increas- 
ing wariness of strangers. Prior to this time they would display 
active and passive submission toward a stranger, but after 18 
months of age, an increasing flight tendency was apparent, more 
so in the male wolf of the pair. Between 2 and 3 years of age, this 
male became increasingly wary of strangers, but if the person was 
introduced by the author and remained passive in a squatting posi- 
tion, the male wolf would eventually approach and investigate, 
vasdllating between active and passive submission and flight. The 
female at this age would usually approach a stranger after a brief 
period of ambivalence to investigate, greet, and solicit petting. The 
female was more exploratory even at 3 weeks of age, and at 4 years 
of age showed more positive social responses and less fear toward 
strangers than the male. 

During the heat period at 2 and 3 years of age, this female 
showed less passive submission and displayed aggression toward 
one of the male golden jackals in the opposite cage particularly at 
these times. After 2 years of age, the male wolf began to threaten 
certain visitors and at 3 years attempted to attack one student. All 
agonistic behavior was directed against male human beings, never 
against women. The possibility that the male wolf is making a 
sexual discrimination, and upon what basis (possibly olfactory), 
warrants further study. 

A third female wolf recently raised in the same way developed 
an inaeasing fear of strange male humans after 5-6 months of age; 
adult females and preadolescent children were readily accepted 
even 6 years later. This pattern has been confirmed by others who 

Socialization Patterns in Wild and Domesticated Canids 


domestic dog, sexual maturity is attained as early as 6 months of 
age, but there is a delay in appearance of territorial behavior and 
aggression toward strangers (both conspecifics and people) until 12 
to 18 months of age, and in some cases up to 2 years. This latter 
behavior may be hormonally dependent since early castration or 
ovariectomy may prevent such behavior from developing (Brun- 
ner, 1968). In the dog therefore, domestication may have caused a 
split in the timing of gonadal and central nervous system matura- 
tion and integration, precocious sexual development being one 
selected attribute in domestication. 


The marked discrimination of human sexuality by some of ^e 
Type n and ni canids only emerged with increasing sexual mata- 
rity. As far as could be ascertained, male assistants did not ^^^at 
the animals and treated them in a comparable way o / 

dress was also often identical, both sexes having long air an 
jeans! This sex discrimination was most marked in e m e 
and the male golden jackal, overt aggression being ‘°- 

ward strange males at increasing frequency a er 2 y . . j 
The author was attacked by a male wolf dunng the ftirmng of 
the “Wolf Men," a television (NBC) , , been 

stranger to this wolf, which, together wit 1 s ( Iban its 
hand-raised but had infrequent contact wit pe^ 
handler. Prior to releasing the two wolves from *eir cage for him 
ing in a large enclosure, the female, -'ho was m heat, sobated 
author through the cage with full vagina) disp ay repeatedly 

The male wolf intercepted her, 

threatened the author. When released, xhis example 

tacked the author (for further details see 

Illustrates clearly one of the problems o ^eact toward 

a consequence of socialization, they wo 

human beings in a reviewed m exlat$o by 

normally react to conspecihcs (this ^ ^ ,be attack was 

Fox, 1968c, 1971b); the most logical the 

that the author represented a s^xua pences of socializa- 

attentions of the female. More exlrem 


THE dog: its domestication and behavior 

gression, in contrast to the purely offensive display toward 

Experiments moving coyotes from one enclosure to another 
and rearranging pairs has revealed a tendency for females to be 
more aggressive toward strange male and female conspecifics than 
their male partners. A strange adult male, dominant to the resident 
female but subordinate to the resident male 6 months after intro- 
duction, caused a dramatic change in the pair-bond. The female 
developed an allegiance with the strange male, who became domi- 
nant over her original partner, but in her absence remained sub- 
ordinate. Any female coyote placed in the cage with these animals 
would only be attacked by this resident female. The possibility that 
the dyadic relationship in the coyote is matiifocal (in that the 
female is the controller and selector of the partner and regulates 
intraspedfic proximity) deserves further analysis in the field. 

In the red fox, wariness of strangers was consistently seen as 
early as 4 months of age, and in only one instance was active 
submissive greeting displayed toward a person other than that 
who had been responsible for hand-rearing. This lack of generali- 
zation clearly demonstrates the limited capacity of the red fox to 
develop secondary social relationships. 

It should be emphasized that all subjects had more or less the 
same exposure to people after weaning had been completed be- 
tween 3 to 4 weeks of age. 


With the exception of the red fox, many of the above changes in 
behavior correlate with the attainment of sexual maturity. The 
Type II and III canids show a gradually increasing tendency to 
avoid strangers after 4 to 5 months of age, which is clearly evident 
at 12 to 18 months and tends to persist. In captivity, the female 
coyotes have shown estrus at 10 months of age, although they do 
not normally show estrus or breed until the second year of life. The 
female wolf had her first heat at 2 years, the male showing little 
interest until the following year. The later emergence of defensive 
and offensive aggression rather than avoidance reactions toward 
strangers may be related to this late sexual maturation. In the 

Socialization Patterns in Wild and Domesticated Canids 

mally leads to dispersion around 5 months of age in the Type I 
canids and around 10 months in the Type II canids (Fox, 1975). In 
the more sociable Type III canid, the care-dependency relationship 
gives way to a dominance-subordinate relationship combined with 
allegiance and affection (Fox, 1972). The capacity to form secondary 
social relationships and to form a stable social hierarchy is limited 
in the Type II canid and more or less absent in the Type I solitary 

Compared to the domestic dog, the wolf seems to have a lesser 
capacity to form secondary social relationships. There may be a 
period after which such relationships are difficult to establish in the 
wolf. This may be correlated with the fact that the wolf pack, espe- 
cially the upper echelon of mature dominant wolves, is closed to 
strange wolves. Strangers are avoided or driven away, while lower 
ranking yearling wolves will more readily accept strangers and 
may even leave the main pack (Fox, 1973)' social behavior of 
the more mature wolves is an ecologically adaptive sodal 
mechanism that regulates pack size. In the domestic dog, this e- 
havior may have been selectively eliminated in many breeds so that 
as adults they will readily accept strangers. The possibility of infan- 
tiUsm (Zimen, 1970) or neotenic perseverance of infantile care- 
solidting and submissive behavior in the domestic dog may aci 
tate the generalization of secondary sodaiization as well as inaeas- 
ing proximity tolerance. Most significant, however, is * ^ 
for innate sodal predispositions which may fadUtate t e ’ 

cation of some spedes but be a major limiting factor in o ® 

different temperament and capadty to develop secon ary so 


The sodal consequences of hand-rearing have 

their actions to their foster parent and to ot er ■ socio- 

been reviewed. The canids studied ^ .md 

ecological types, namely J D^fferencfs in permanence 

intermediate coyote and golden sccondarv' social 

of primary sodal attachments, capaatj t 


THE dog: its domestication and behavior 

tion are well illustrated in various spedes of birds (Klingbammer, 
1967) and zoo animals (Hediger, 1950) which, when hand-raised, 
later show a marked sexual preference for human beings. The con- 
sequences of sodalization with man are less dear-cut in the various 
canid spedes. All types studied remained attached to the person 
who hand-raised them up to their current age of 4 years.* The 
solitary Type I canid shows a limited capadty for generalization or 
for the formation of secondary social relationships. This correlates 
well with the socio-ecology of this Type (Fox, 1975). Several indi- 
viduals of Type n showed a lesser capadty to form secondary social 
relationships compared with the wolf. Recent observations of 
dingos reveal a similar Type II pattern of sociability, a finding ver- 
ified by Corbett and Newsome’s (1975) field study of their social 
ecology. There is evidence that the Cape hunting dog, another 
Type HI canid, also has a considerable capadty to form secondary 
social relationships with people after being hand-raised. People 
who have hand-raised Mexican wolves report that their sodaliza- 
tion patterns resemble the coyotes more than the typical wolf. This 
accords well with the social ecology of this subspedes (Cams lupus 
baileyi) which is closer to the coyote in social behavior, rarely form- 
ing packs and more commonly being seen alone or in pairs. 


The main conclusions of this study are summarized in Table I. In-a 
review of sodalization problems in various nondomesticated, 
hand-raised carnivores such as ocelots and raccoons (FoX/ 1972)/ a 
common finding is increasing aggression and unpredictability of 
behavior toward strangers, and increasing intolerance when disd- 
plined by the owner. The change from the care-dependency rela- 
tionship of the primary sodal attachment to a more independent 
relationship is typical of the relatively solitary carnivores 
(exemplified by the red fox in this study). Increasing proximity 
intolerance and parent-infant and infant-infant aggression nor- 

•Incrcasod aggression and assertion of rank, especially during the breeding season 
may not be evident in the wolf until 4 to 5 years of age in both males and females. 


Stages and Periods in 
Influences and 


The purpose of this chapter is to review a number 
serve to illustrate various principles of neural and e 
velopment. An attempt is made to bring together severa i 
topics from the ethological and psychological literature 
formulate some general concepts pertaining to t ® . 

interpretation of critical and sensitive penods m e P 
These periods represent developmental stages a w inne- 

mental (i.e., human) influences can have .'“"t 

lasting effects upon later behavior, phys'°'°^' to describe 

tivity. A number of terms in current use that P . ■ 

some of these developmental phenomena are ^ 

to clarify the use of such terminology in this someiv ‘ ^1 

of developmental psychobiology. Structura an . ^,5 of 

velopment of the ca^ne brain is correlated -'h 
behavioral ontogeny underlying the critical pen 



THE dog: its domestication and behavior 

relationships, changes with sexual maturity and socio-sexual dis- 
criminations are discussed. The various relationships between so- 
cialized canid and man reflect the innate social capacities of the 
species in question and also correlate with the socio-ecological pat- 
terns of the species under natural conditions. In other words, it is 
shown that the socio-ecologically adapted temperament and social 
capacities of each canid type are primary determinants of their 
reactions toward human beings after early socialization with man. 
Where relevant, the social behavior of domesticated dogs is com- 
pared and contrasted with that of the wild species; in contrast to 
the dingo and wolf (proposed ancestors of C. familiaris), most 
breeds of dog have a greater social potential or ability to establish 
secondary social relationships which, in contrast to these other 
species, must be a consequence of domestication per se. 

Stages and Periods in Development 


Also, the size and elaboration of the processes of fibrous astrocytes 
closely resemble the adult between 5 and 6 weeks of age (Fox, 

From these observations, it is apparent that neocortical 
neuronal maturation precedes myelinization and that the second 
myelinogenetic cycle does not begin until neuronal and glial de- 
velopment is well advanced. 

Detailed quaBtative studies on the postnatal development of 
the canine EEG during wakefulness, quiet sleep, and paradoxical 
(REM or activated) sleep show that the first signs of slow wave 
(possibly thalamocortical) activity appears around 17 days, and by 4 
weeks of age, a clear distinction between various states of wakeful- 
ness and sleep can be detected on the EEG (Fox, 1971b). Relatively 
mature patterns of electrocortical activity are present at 5 weeks of 
age, at which time the percentage of various states of sleep and 
wakefulness are relatively mature. Only slight qualitative changes 
in EEG occur after 5 weeks of age, notably the preponderance of 
fast spindle activity at the onset of quiet sleep, a gradual reduction 
in amplitude and increase in fast frequency components during 
wakefulness, and a more gradual increase in amplitude during 
drowsiness and quiet sleep. In close temporal association with EEG 
development, auditory and visual evoked polenHals, in terms of 
latency, attain mature characteristics between 5 and 6 weeks of age. 

Behavior Development in the 

Several parameters of behavioral development in this species have 
been investigated and correlate well with the above data on ChJS 
development. The dog is neurologically mature at 4 weeks of age 
with the exception of equilibration and adult locomotor abilities 
such as running and leaping (Fox, i9;nb). Between 3 and 4 weeks of 
age the pup begins to interact with its socioenvironmental milieu 
and to develop primary social relationships or emotional attach- 
ments. This marks the onset of the critical period of socialization 


THE dog: its domestication and behavior 

The degree of plasticity and adaptability of the developing 
brain and behavior can be evaluated, for example, by environmen- 
tal manipulations such as sensory deprivation, social isolation, or 
excessive stimulation (handling, experiential enrichment) at dif- 
ferent ages or stages of development. These various treatments that 
may modify brain and behavior development are considered in 
relation to animal domestication. 

Structural and 

Functional Development of the 
Canine Brain 

Myelinization of the canine central nervous system (CNS) occurs in 
two cycles. At birth and during the first 3 weeks, there is a gradual 
increase in myelin content of the spinal cord occurring earliest in 
the cervical region and in motor roots prior to sensory roots. The 
corticospinal tract is the last major efferent pathway to develop. 
Subcortical structures posterior to the posterior commissure also 
begin to myelinate during this early postnatal period (Fox, 1971a). 
Cranial nerves associated with feeding and cephalic cutaneous 
sensitivity (facial and trigeminal nerves) and with balance and 
body-righting (nonacoustic portion of the 8th cranial nerve) are 
well myelinated at birth. Between 3 and 4 weeks of age, the second 
cycle of myelinization occurs, anterior to the posterior commissure; 
specific and nonspecific thalamocortical afferent fibers become 
myelinated (Fox, 1971a). The various regions of the neocortex do not 
show an equal increase in myelinization. Myelin is first detected in 
the somatosensory area at 4 weeks and by 6 weeks of age is more 
evenly distributed in other regions such as the visual and auditory 
cortex. The frontal lobe shows the most gradual myelinization. 

In contrast to this more gradual myelinzation of the neocortex, 
neuronal development in terms of cell density, neuronal size, and 
apical and basilar dendritic complexity, attains relative maturity in 
the sensorimotor, visual, and auditory cortex by 6 weeks of age. 

Stages and Periods in Development 


with the mother but with a human being, a flashing red light, or a 
moving cardboard box, they become preferentially attached to the 
species or the object with which they have been raised. Some re- 
versal is possible during subsequent weeks, but there is strong 
evidence that this early exposure results in a very specific and 
enduring attachment — so enduring that at maturity social and sex- 
ual behavior may be directed toward the same stimulus to which 
the bird was imprinted early in life. 

Lorenz (1970) hand-raised jackdaws and crows and found that 
when they reached maturity they would show courtship behavior 
toward him and would attempt to mount his hand. During the 
time when they would normally be taking care of their own young, 
they would attempt to stuff grubs into his ears. Hediger (1950) 
describes the experience of one of his zoo keepers who hand-raised 
a male moose. When the moose reached sexual maturity, the 
keeper led it into a field of female moose, and the young bull 
became sexually aroused. Instead of directing his sexual behavior 
toward a female moose, however, he attempted to mount his 
keeper. Such bizarre behaviors are good examples of the enduring 
effect of imprinting in determining later social and sexual prefer- 
ences in various animals. Klinghammer (1967) has shown that the 
effects of hand-rearing in various species of pigeons can vary. One 
species, for example, if hand-raised, shows a sexual preference at 
maturity exclusively for its human handler rather than for its own 
species. Other closely related species show a reversal at maturity; 
although still friendly toward the human foster parent, they are 
only sexually attracted to their own species. Klinghammer also 
identifies a third category of pigeons in which individuals have the 
best of both worlds and show sexual behavior toward both their 
own species and the foster parent! 

It is also known that the hvo sexes of a given species arc not 
affected in the same way by imprinting. In mallards, for example, 
Schutz (1965) finds that early imprinting in the males later deter- 
mines their sexual preference while female mallards, regardless of 
imprinting, show an innate preference for males of their own 
species. This was confirmed by raising male and female mallards 
with different species of ducks. When they reached matunty, the 
male mallards preferred the species with which they had tx'en 


THE dog: its domestication and behavior 

(Scott and Fuller, 1965), and the neurological and behavioral events 
are briefly reviewed since they are important factors which under- 
lie the beginning of the critical period. 

The data on the developing canine brain serve to demonstrate 
the temporal coincidence of development and maturation of sev- 
eral interrelated structural and functional parameters. This coinci- 
dence, which occurs between the fourth and fifth postnatal week in 
the dog, may be termed a period of integration. It is at this time 
that the several parts of the developing nervous system show both 
structural and functional integration, which marks the beginning 
of a relatively mature organizational level of activity. 

At this time, the organism begins to interact rather than react 
with conspecifics and through social experiences with both parent 
and peers develops emotional attachments to its own kind or to 
man. If denied human contact during this critical period from 4-12 
weeks of age, it will subsequently avoid human contact (Scott and 
Fuller, 1965). Such dogs are fearful of humans and are virtually 
untrainable. The fear period which develops after 8 weeks of age 
limits the capacity to develop new social attachments and essen- 
tially terminates this critical socialization period. Thus even in a 
domesticated species, lack of exposure to man during this forma- 
tive period (when brain centers are integrating and emotional reac- 
tions developing) will greatly limit the social potentials of the 

Imprinting and 

The concept of a critical period implies that experience at a particu- 
lar time of development is essential for normal development to 
continue. This is exemplified by the phenomenon of imprinting in 
birds. Imprinting means attachment, and birds (such as ducklings) 
that are relatively mature when hatched normally become im- 
printed onto the mother during the first few hours after hatching. 
If they are taken as soon as they are hatched and are raised not 

Stages and Periods in Development 


used three groups. One group was hand-raised exclusively with 
people. The second group had contact only with other monkeys. 
The third group had more or less equal contact with humans and 
their own Idnd. The monkeys segregated into like groups lor social 
play during early life and later clearly demonstrated sexual prefer- 
ences based upon their rearing experience. 

If social experiences are denied during the early critical period, 
as demonstrated in our cat-dog socialization study, there is often 
impairment in the subsequent development of social relationships. 
Scott and Fuller (1965) showed that if dogs are denied human con- 
tact until approximately 14 weeks of age, they are wild and unap- 
proachable. Scott and Fuller demonstrated clearly the critical na- 
ture of the socialization process and found that human contact 
between 6 and 8 weeks of age seems to be optimal for the socializa- 
tion of dogs (see Figure 1). 

Although there is an optimal period for socializing pups, there 
is evidence that dogs may subsequently regress or become feral. 
The social bond with man may be broken when well-socialized 
pups are placed in kennels at 3 or 4 months of age; by 6 or 8 months 
they are shy of strangers and often of their caretakers if they have 
not been handled much. In addition, they may be extremely fearful 
when removed from their usual quarters. Their fearfulness is the 
result of a combination of institutionalization and desodalization. 

In connection with the phenomenon of desodalization, Woolpy 
(1968) found that captive wild adult wolves can be sodalized in 6 
months of careful handling and that when they are subsequently 
given less human contact they do not regress or become deso- 
dalized. In contrast, wolves that are sodalized early in life are like 
dogs in that they will regress if they are subsequently given less 
human contact. These findings suggest, therefore, that although 
there is an optimal period early in life when sodalization can be 
rapidly established, subsequent reinforcement is necessary be- 
cause of some intrinsic instability of retention in young animals. 
Woolpy (1968) concluded that 

an important aspect of sodalization is learning to cope \dth a 
previously unfamiliar enviroiunental situation in the presence 
of unreduced subjective fear. . . . We have inteq^reted the re- 
sults of both the tranquilizer and the sodalization experiments 


THE dog: its domestication and behavior 

cross-fostered while the female mallards tended to reverse their 
social preference in sexual encounters and to seek out males of 
their own species. 

Dogs have been raised with cats during the critical period of 
socialisation to evaluate further the effects of cross-fostering. In 
this study a 3-week-old Chihuahua was placed with a litter of 
4-week-old kittens. Five replications of the study were done (Fox, 
1971a), and in each replication a battery of tests was given to the pup 
at 12 weeks of age. It was found that the pups raised with kittens 
made no social responses to their own mirror images; they literally 
lacked species recognition. They also preferred the company of cats 
to that of the littermate Chihuahuas which were used as controls. 
The cats that had been raised with a dog were also sociable toward 
dogs that had not been raised with cats. In contrast, cats that had 
had no earlier exposure to dogs avoided contact with them — with 
one exception. Salzen and Cornell (1968) did a comparable study 
for color preferences in chicks, which is reminscent of the role 
integrated schools might play in achieving interracial socialization. 
They raised a green-dyed chicken with a group of red-dyed chick- 
ens. When they placed these chickens together with a new group 
of chickens that were all dyed green, the green chicken ran toward 
his red companions and ^d not mix with the green group. Var- 
iations on this experiment seem to confirm that allegiances and 
social preferences are based on early social learning. 

Even more subtle consequences of early rearing can affect so- 
cial preferences. One experiment used three groups of pups. The 
pups in one group were hand-raised and were exposed only to 
humans. The pups in the second group were weaned early and 
had almost equal contact with humans and dogs up to the point of 
testing. The pups in the third group were raised with eadi other 
(Fox, 1971a). When the pups were placed in new social groups, it 
was found that they tended to segregate themselves in accordance 
with their rearing history. The pups that had been hand-raised and 
had no social experience with their own kind tended to stay together 
while the pups that were weaned early and the controls tended to 
segregate into like groups. Other aspects of social behavior were 
affected also. 

Sackett et al. (1965) found a very similar social consequence of 
early rearing experiences in young rhesus monkeys. They too 

Stages and Periods in Development 


used three groups. One group was hand-raised exclusively with 
people. The second group had contact only with other monkeys. 
The third group had more or less equal contact with humans and 
their own kind. The monkeys segregated into like groups for social 
play during early life and later clearly demonstrated sexual prefer- 
ences based upon their rearing experience. 

If social experiences are denied during the early critical period, 
as demonstrated in our cat-dog socialization study, there is often 
impairment in the subsequent development of social relationships. 
Scott and Fuller (1965) showed that if dogs are denied human con- 
tact until approximately 14 weeks of age, they are wild and unap- 
proachable. Scott and Fuller demonstrated clearly the critical na- 
ture of the socialization process and found that human contact 
between 6 and 8 weeks of age seems to be optimal for the socializa- 
tion of dogs (see Figure i). 

Although there is an optimal period for socializing pups, there 
is evidence that dogs may subsequently regress or become feral. 
The social bond with man may be broken when well-socialized 
pups are placed in kennels at 3 or 4 months of age; by 6 or 8 months 
they are shy of strangers and often of their caretakers if they have 
not been handled much. In addition, they may be extremely fearful 
when removed from their usual quarters. Their fearfulness is the 
result of a combination of institutionalization and desocialization. 

In connection with the phenomenon of desocialization, Woolpy 
(1968) found that captive wild adult wolves can be socialized in 6 
months of careful handling and that when they are subsequently 
given less human contact they do not regress or become dcso- 
cialized. In contrast, wolves that are socialized early in life arc like 
dogs in that they will regress if they arc subsequently 
human contact. These findings suggest, therefore, that although 
there is an optimal period early in life when socialization 
rapidly established, subsequent reinforcement is nccessaiy be- 
cause of some intrinsic instability of retention in young animals. 
Woolpy (1968) concluded that 

an important aspect of socialization is learning to cope with a 
previously unfamiliar environmental situation in the presence 
of unreduced subjective fear. . . . We have inte^reted the re- 
sults of both the tranquilizer and the sooaliz.alion experiments 

response score ? 

3 5 7 9 


Figure i. Socialization in the dog involves an initial attraction 
phase, but if denied human contact until first tested at 5, 7, or 9 
weeks of age, fear and the tendency to flee increases with increasing 
age. The optimal penod for socialization is between 6 and 8 weeks. 
(Adapted from Scott and fuller, 1965.) 

to indicate that the fear of the unfamiliar is the primary obsta- 
cle to wolf socialization and that, whUe the overt responses of 
fear appear very early in life, its subjective components con- 
tinue to develop throughout at least the first year. Socializa- 
tion must be conditioned in the presence of the fully de- 
veloped subjective components of fear, and hence it cannot be 
permanently maintained in juveniles if they are left to develop 
fear responses subsequent to having become socialized in early 

There seems to be a comparable critical period for the de- 
velopment of emotional attachments in children. Bowlby (1971)/ 

Stages and Periods in Development i6i 

from the Tavistock Clinic in London, has placed much emphasis 
upon the critical nature of infant socialization in determining later 
socially adjustive behavior and in preventing delinquency and 
even antisocial and sociopathic behaviors. It seems that in both 
animals and humans the initial or primary socialization early in life 
is the basis for the development of subsequent secondary social 
relationships; if primary attachments are not made or are in some 
way modified, the consequences for the later social adjustment of 
the individual can be quite serious, and in terms of domestication 
greatly limits the potentials of the animal for human use. 

Socialization and 

The ''perpetual puppy" syndrome may develop in adult dogs if a 
symbiotic relationship has been maintained by overindulgent and 
permissive owners, and severe anaclitic depression may follow 
separation of the dogs from their owners for surgery, boarding, or 
quarantine (Fox, i968d). It should be emphasized that as a conse- 
quence of the Symbiotic relationship with the owner the pet may 
develop a variety of care-soliciting (et-epimeletic) reactions such as 
whining, jumping up, following constantly throughout the house, 
crying when left ^one, and submissive urination. These symptoms 
resemble regression in man to more neotenic or infantile behaviors. 
Punishment after the disturbed pet (or child) has urinated, defe- 
cated, or generally pestered the owner sufficiently may lead to a 
masochistic form of reinforcement. 

‘"Sympathy" lameness, hysterical paraplegia, and coxalgia 
have been described in dogs (Fox, i968d) and are well documented 
in man as attention-seeking reactions. Chess (1969) stresses the 
correlation between acute illness and dependency behavior in 
human infants. After recovery, the child attempts to maintain the 
interpersonal relationship that brought him special attention dur- 
ing the illness. Some overindulged pets have been kno^vn to refuse 
to use one limb after surgery for congenital patella luxation because 
they received so much attention and petting from (heir owners 

i 62 

THE dog: its domestication and behavior 

while they were recovering. In extreme cases, muscle atrophy de- 
veloped; in others, surgical recovery was complete, but the sub- 
jects would suddently become lame when they were in an anxiety 
or conflict-provoking situation and were soliciting the attention of 
their owners. 

Environmental and 
Experiential Influences 

Environmental and experiential factors which influence develop- 
ment are reviewed briefly to provide a basis for further discussion 
of the importance of environmental influences in the process of 
animal domestication. 

Schneirla (1965) has developed a very important theory involv- 
ing the significance of approach-withdrawal processes in the or- 
ganization and development of behavior. For instance, approach 
and subsequent reward (such as contact comfort) are tied in with 
parasympathetic arousal, while withdrawal from painful stimula- 
tion is associated with adrenal-sympathetic arousal. Contact com- 
fort, especially that associated with nursing or petting an animal, 
causes parasympathetic arousal (exemplified in the human infant 
by salivation, increased peristalsis, secretion of digestive juices, 
general relaxation, and occasionally penile erection). Young ani= 
mals derive considerable reward from contact comfort, grooming, 
and nursing; if the same circumstances cause parasympathetic 
arousal, then contact comfort, grooming, and nursing would tend 
to improve digestion and assimilation of food as well as to facilitate 
emotional attachment (Fox, 1975b). This "gentling" or petting phe- 
nomenon is part of the taming-domestication process. Even gen- 
tling a pregnant animal can result in offspring that are more docile, 
and as emphasized by Denenberg and Whimbey (1963), this may 
be a significant fact in the domestication process. 

Several years ago Spitz (1949) demonstrated that inadequate 
mothering, which may be reinterpreted as inadequate parasym- 
pathetic arousal, led to a wasting disease in many orphan children. 

Stages and Periods in Development 


These children did not gain weight, did not adequately digest and 
assimilate their food, and many succumbed to infections. When 
Spitz initiated a regime of mothering, the infants began to gain 
weight, and the rate of mortality decreased significantly. This ef- 
fect, distinct from the handling effect, has been termed gentling. 
Bleicher (personal communication) has found similar effects 
in handled and nonhandled orphan pups raised in social isola- 
tion.* No hormone has yet been identified, but it is possible 
that the gentling of pregnant rats influences the parasympathetic 
nervous system and that certain neurohormones affect the develop- 
ing fetus. 

A number of independent studies on rodents supports 
Schneirla's theory, demonstrating that experimental manipula- 
tions early in life can have long-lasting effects on later behavior. 
For instance, if a 5-day-old rat is taken out of its nest and is placed 
in a metal pot at room temperature for 3 min a day for 5 days and 
then is allowed to mature, as an adult it is less emotional than 
littermates not treated in this way. It may also be more resistent to 
physical stress such as terminal starvation, cold exposure, and cer- 
tain pathogens. This effect, which has been called the early han- 
dling effect, seems to influence the adrenal-pituitary axis of the 
developing rodent. Denenberg (1967), Levine and Mullins (1966), 
and other workers have studied this phenomenon in great detail, ft 
would appear that the stress to which the neonate is exposed in 
some way affects the way in which it responds to psychological 
and physical stresses later in life. It has been proposed that a hor- 
monostat exists in the neurohypophysis which is "tuned" to the 
adrenal glands during the sensitive period when the rat is between 
5 and 10 days of age. When this is tuned experimentally by a 
sudden elevation of corticosteroids during the sensitive period, the 
hormonostat operates differently when the organism is stressed in 
maturity. Typically, as Levine has demonstrated, the stress re- 
sponse in adult control rats is somewhat maladaptive. There is a 
long latency period before the neuroendocrine system responds, 
but the eventual response can be long-lasting and at times may 

These effects have also been found in calves (Professor C. Schivabc, personal 
communication). Mortality rates were lower on farms where calves were handled 
more ofter> and with more care and affeebon. 


THE dog: its domestication and behavior 

trigger the onset of Selye's stress syndrome. Rats handled early 
have a much shorter latency of response, and the duration of re- 
sponse is shorter. In effect, their reactions are not unduly delayed 
and they do not overreact. 

In some strains of mice that develop spontaneous leukemia, 
the onset of the condition can be delayed by this handling proce- 
dure. Handled mice also have a greater resistance than nonhan- 
dled controls to Implanted tumors. There are also genetic or strain 
differences, as demonstrated by Ginsburg (1968). For one strain, a 
given level of stimulation might be excessive; in another strain, the 
sensitive period might lie between postnatal days 6 and 10 or be- 
tween postnatal days 10 and 15. Ginsburg emphasizes that in a 
typically heterogeneous population, as in Homo sapiens, there 
would be a normal distribution curve and that individuals would 
have different sensitive periods as well as different response 
thresholds. In view of these individual and genetic variations, 
therefore, we must be very careful in making generalizations about 
the handling effect. 

Levine points out that in the relatively "overswaddled" labora- 
tory environment neonate rats may well be understressed and 
that the handling procedure is much closer to the kind of experi- 
ence they would normally have in the wild. Under natural condi- 
tions, the mother frequently leaves the nest to forage for food, and 
there are various environmental changes, all of which could have 
an additive effect resulting in an adult animal that is psychophysio- 
logically superior to the "overswaddled" laboratory specimen. 

In a study of the handling phenomenon in dogs (Fox, 1971a), 
pups were subjected to varied stimulation — exposure to cold, ves- 
tibular stimulation on a tilting board, exposure to flashing lights, 
and auditory stimulation — from birth until 5 weeks of age. The 
pups in the study differed from the controls in a number of ways 
including earlier maturation of EEG, lowered emotionality which 
enhanced problem-solving ability in novel situations, and domi- 
nance over controls in competitive situations. Analysis of their ad- 
renal glands indicated a fivefold increase in norepinephrine, and 
studies of their heart rates indicated that a greater sympathetic tone 
was developed as a consequence of the early handling stress. Meier 
(1961) demonstrated comparable maturation of EEG and behavioral 
changes in superstimulatcd Siamese kittens. (See Chapter 10.) 

Stages and Periods in Development 


A generalization cannot be made about optimal handling for a 
given species. For instance, it appears possible that a given level of 
early stimulation may produce psychophysiological superiority in 
some human infants and pathophysiological inferiority in certain 
other individuals. As Thomas et al. (1970) have demonstrated in 
their longitudinal studies of human infants, handling has to be 
very carefully adjusted to the basic temperament and autonomic 
tuning of the individual. The effects of early handling appear to be 
on the adrenal-sympathetic system, and the research evidence 
suggests that early handling not only resets the pituitary-adrenal 
axis but in some way influences autonomic tuning and tempera- 
ment or emotionality. 

To what extent current animal husbandry practices and vari- 
ous handling regimes adopted in early domestication affect farm 
livestock and house pets alike, remains to be evaluated. Those 
breeders who have adopted the above handling stress program for 
puppies and also the U.S. Army Veterinary Corps (Biosensor Re- 
search Division) report extremely promising results in terms of 
later stress — resistance, emotional stability, and improved learning 
ability. This phenomenon may represent a new tool in animal hus- 
bandry and domestication. 

Prenatal Influences 

Prenatal anxiety can have a significant effect on the emotionality 
and the later personality developed of an infant (JoHq, 1969). 
Thompson (1937) was one of the first to demonstrate the effects of 
prenatal anxiety on the behavior of offspring. He developed a con- 
ditioned emotional reaction in rats placed in a shuttle box; 
whenever a bell rang, the rats had to jump to the safe side of the 
box in order to avoid shock. The basis for an emotional reaction 
was established by placing a barrier in the center of the box so that 
the animals could not jump to the safe side when the bell rang. 
Since the rats were never given shock when the bell rang after the 
barrier was erected, the reaction was purely emotional. The off- 
spring of pregnant rats that were stressed in this way were cross- 
fostered by normal mothers in order to control for any postnatal 


THE dog: its domestication AND BEHAVIOR 

transfer effects from the mother. Thompson found that the prenat- 
ally stressed rats were much more inferior because heightened 
emotionality interfered with their performance. He was able to 
produce a similar effect by injecting adrenalin and ACTH into preg- 
nant females. 

Joffe (1969) has reviewed many such experiments including his 
own on the Maudsley reactive and nonreactive strains of rats. He 
was able to demonstrate genetic differences in susceptibility to 
prenatal stress as well as differences correlated with the sex of the 
offspring and the period during pregnancy when the stress was 
administered. He discovered that premating stress could also have 
a significant effect on the behavior and the reactivity of the off- 
spring. These experiments emphasize that the developing 
phenotype is modifiable not only after birth but also prenatally, the 
effect being mediated by the neuroendocrine system. 

These prenatal and postnatal studies in modifying the 
phenotype also show that relatively little is known about how to 
provide environmental stimulation and rearing programs which 
will ensure that the developing phenotype can be optiiruzed or at 
least how it can be protected from deleterious influences in food- 
producing farm animals. There is much discussion about genetic 
engineering and programmed breeding through artificial insemina- 
tion, but the effects of environmental phenomena that are present 
during certain critical periods in development have barely begun to 
be explored. 

Environmental Enrichment and 

In The Descent of Man, Darwin observed that the domesticated rab- 
bit has a much smaller brain than its wild counterpart and attrib- 
uted this to the cumulative effect of generations of captivity during 
which each generation received far less stimulation than it would 
have in the wild. To test the effect of environmental stimulation on 
captive animals, Bennett and his co-workers (1964) at the Lawrence 

Stages and Periods in Development 


Radiation Laboratory in California raised rats in enriched environ- 
ments. Typical laboratory rats were placed in a large cage with cage 
mates and with various objects (wheels, runways, and so on) to 
manipulate. Under these conditions of environmental complexify, 
Bennett found that the rats in the study became more exploratory 
than the controls and that they developed significant differences in 
brain size, in the depth of the visual cortex, and also in the turn- 
over rates of brain acetylcholinesterase. More recently Bennett 
demonstrated that the enrichment effect is dependent upon an 
interaction between the inanimate environment and conspecifics. 
That is, if a rat is raised alone in an enriched environment, pro- 
found changes in brain and behavior do not occur; nor do they 
occur if a rat is raised with companions in a barren cage. 

Dogs have been raised under a schedule of paced increments 
of experience, periodically taking some of them out of their home 
cages and letting them explore an arena containing novel stimuli 
(Fox, igyia). Those that were allowed in the arena at 5, 8, 12, and 16 
weeks of age for a mere V2 hr per exposure explored increasingly as 
they grew older and developed a preference for more complex 
stimuli as they matured. Litfermates that were placed in the arena 
for the first time at 12 or 16 weeks of age did not explore; they 
withdrew or did not leave the start chamber, and many of them 
were catatonic with fear. We are dealing here with an in- 
stitutionalization syndrome; those dogs that did not have an op- 
portunity to leave their home cages until sometime after 8 weeks of 
age could not tolerate the complexity of the environment and so 
they withdrew to avoid overstimulation. (Later some of the neuro- 
logical effects of the emergence from isolation are discussed.) Sac- 
kett (1968) adds support to our canid study in an experiment that 
he did with rhesus monkeys. He found that as rhesus monkeys get 
older, they prefer to look at picture cards of increasing complexity. 

If monkeys are raised in isolation, at 6 months of age they prefer to 
look at cards of less complexity than those which rhesus monkeys 
normally prefer at that age. He concludes from these experiments 
that in the absence of paced increments of experience the organism 
will seek a lower level of stimulation and environmental complexity. 

From these studies an arousal-maintenance model of 
perceptual-motor homeostasis can be formulated wherein the op- 
timal arousal or tolerance level is set early in life as a result of the 


THE dog: its domestication and behavior 

quality and quantity of early experiences. The level is set low in 
those animals that have had few increments of experience. If the 
environment does not provide varied stimulation, the subject may 
compensate by creating its own varied input by elaborating 
stereotyped motor acts or by directing specific activities toward 
inappropriate objects (such as copulating with its food bowl). The 
stereotyped motor acts (thumb-sucking, self-clutching, and rock- 
ing in primates) developed while in isolation may be performed 
when the subject is in a novel environment and may serve to re- 
duce arousal or anxiety because they are familiar acrivities and may 
be comforting (Berkson, 1968). This type of stereotype is to be 
distinguished from the locomotor cage stereotypes described by 
Meyer-Holzapfel (1968) which are derived from thwarted attempts 
to escape. Mason (1967) has developed a comparable theory in 
which he uses the term "general motivational state" in reference to 
the influence of the degree of arousal on the organization of be- 
havior during different periods of development. 

In reviewing their own studies of primates, Jensen and Bobbitt 
(1968) show how the deprivation of inanimate play objects affects 
social behavior. 

Inanimate objects constitute another important class of 
environmental factors. Our tests of the effects of enrichment 
by toys indicate that lack of them and climbing facilities will 
seriously handicap the young animal in learning motor skills, 
in developing independence from its mother, and in interact- 
ing with peers. Further, these effects may be critical in deter- 
mining later social dominance. We hypothesized that prior and 
concurrent toy experience facUitate peer socialisation. 

In an impoverished environment such as a barren cage, there 
IS a prolonged period of mother-infant closeness which is essen- 
tially a retardaHon in the mutual independence process. Mother- 
infant pairs in an enriched environment manipulate themselves 
"'"a manipulate the environment more. Jensen 

and Bobbitt (1968) propose a conHnuous process of detachment of 
infant from mother (and vice versa) as attachments to the larger 
environment develop. Apparently deprived infants at 6 months of 
age are severely handicapped in social responsiveness when faced 
with an ennched peer, with respect to whom they are subordinate. 

Stages and Periods in Development 


These authors emphasize that short-term maternal separation or 
isolation from an enriched environment may actually intensify in- 
teraction when the infant is returned. This temporary increase in 
responsiveness after a brief period of separation (in effect, an in- 
stance where absence makes the heart grow fonder) clearly shows 
the importance of the duration of deprivation in addition to the 
type of deprivation and the age of the organism when deprivation 

As in all developmental problems, the role of genetic factors 
must be considered first. Henderson (1970) has demonstrated ele- 
gantly the interaction between genetic and environmental m u- 
ences in the development of mice. Working with several strains, e 
found that the results with mice raised in enriched environmen s 
were somewhat similar to those obtained by Bennett an ® ^ 
leagues (1964). The mice were superior to the controls 
standard laboratory conditions in performance tests , f • 
ious learning tasks and motivational tests of exp ora 
Henderson proposes that there is an environmental rep P 

uirr^nfplu (and ideally) fi(^ 

Figure 2. The domesticated phenotype u . , 

loith the type of environment in which different 

analogous to a process of pseudospeciatton w ^ ^ ^ conse- 

genotypes and phenotypes in the same fitness transitions 

quence of different domestic be critical m terms of 

between (A) and (B) and (B) and (C) tV 

behavioral adaptation. 


THE dog: its domestication and behavior 

erating as a consequence of rearing under the relatively im- 
poverished environment of the laboratory. He has also demon- 
strated that hybrids of the various mouse strains raised under 
standard laboratory conditions performed much better than the 
pure parent strains in various tests pven to them at maturity (a 
typical example of hybrid vigor). When Henderson raised hybrids 
in enriched environments, their performance scores were also 
higher than those of pure strains that were raised under the same 
conditions. Henderson's paper is an important one for everyone 
working with laboratory airimals. The extent to which the various 
artificial environments in which domesticated animals have been 
raised for generations (e.g., home environment for cats and dogs 
and "intensive" systems for pigs, poultry, and calves) have influ- 
enced brain and behavior remains to be evaluated (see Figure 2). 

Influences and 

Although imprinting and socialization influence sexual preferences 
in later life, other factors relevant to domestication and present 
husbandry practices must be considered. Vandenberg (1969), for 
example, has shown that the presence of a mature male mouse 
accelerates sexual maturation in females compared to females 
raised in a unisexed group. There is also strong evidence from wild 
animals raised in zoos that being raised together per se (in 
heterosexual pairs) may in some way inhibit reproduction. This has 
been confirmed experimentally by Hill (1974) who found that pre- 
pubertal familiarity in deer mice delays reproduction in nonsibling 
pairs. Such a reproductive delay, he proposes, may act to reduce 
inbreeding depression and regulate population growth. A third 
phenomenon, the social facilitation of reproduction (by visual, au- 
ditory, or olfactory cues, depending upon the species) known as 
the Darling effect, is pertinent to this review. Animals in social 
isolation or in small social groups have a lower reproductive effi- 

Stages and Periods in Development 


ciency than those in larger groups. A male (e.g., a bull) will have a 
higher sperm count if given access to females compared to one that 
is socially deprived; while females together (e.g., rodents and 
dogs) may show a synchronization of estrus."^ 

These social and developmental influences on reproductive 
physiology and sexual behavior warrant further study in domesti- 
cated animals and serve to emphasize the close relationship be- 
tween neuroendocrine activity and the social environment. 

Sensitive and Critical 

Some of the complexities of ontogeny and integrative activity of the 
brain and behavior are being opened up for future mvestigation 
through these studies that determine the effects of environment^ 
influences on certain aspects of neurobehavioral development. 
Within certain limits, environmental influences can mo^ geneh 
cally predetermined patterns of development and moc^ the later 
manuring phenotype*. The type and intensity 
stimulation may have different effects at different 
berg, 1964) and at different ages in different 

1968). Similarly, environmental and expenenhal dep"™ may 
produce very different effects at various ages ( 3 ““; ^ 9 ^ F°^^"d 
fencer 1060! The integration of structuro-functional compo- 
n^n'^tHntd associates between different systems mj^al^ 

be affected (Riesen, 1961) as weU as producing no p 
ceneral effects such as influencing the general level of arousa , 
fmotit“and“ response threshold to -“c- or nove^tiniuli 
(Denenberg, 1964). Modification of the ® j, 

vironmentfl or experiential ZZn- 

Ppp^"-'"P “pp" •>" 

•Possibly large numbers of animals caged 'n 

fertility^ phenomenon suspect in large breedmg kennels 

:tty may show a dccrcaw in 


THE dog: its domestication and behavior 

of stimulation or deprivation and also the age and strain of the 
species used. 

Isolation, deprivation, or selective stimulation and enrichment 
may alter the normal ontogenetic sequence of behavior develop- 
ment so that certain patterns may disappear earlier with maturity 
or persist for an abnormally long time. Meyer-Holzapfel (1968) has 
shown that with continued reinforcement, the gape response of 
birds may persist and not disappear with maturity at the normal 
time. Later developing patterns may not appear at the normal time 
because of inadequate or conflicting stimulation or reinforcement, 
as shown, for example, by Kovach and Kling (1967) in their studies 
of feeding behavior of kittens fed by stomach tube and deprived at 
various ages from nursing. To evaluate normal ontogenetic processes 
by such techniques may be misleading; what might be shown is the 
degree of modifiability or adaptability of the behavioral phenotype 
within certain sensitive periods and the dependence (or indepen- 
dence) of development and integration upon stimulation, rein- 
forcement, and paced increments of experience. 

A distinction is now drawn between critical and sensitive 
periods because these terms have been used indiscriminately in the 
past to describe temporally discrete periods in an organism's life- 
time when a number of very different experiences such as handling 
(Denenberg, 1964), social experiences (Scott, 1962), and imprint- 
ing stimuli (Bateson, 1969) have their greatest and most enduring 
influence. This distinction is necessary because some experiences 
may be essential for development to continue normally (i.e., ex- 
perienhaUy dependent development); whereas other behaviors 
and organismic functions may not be dependent upon such influ- 
ences for their normal development, yet may be affected at a par- 
ticular time early in life by these environmental influences (i.e., 
development is experientially independent but modifiable). A third 
category of behaviors and functions may be experientially inde- 
pendent and essentially unmodifiable: these are discussed sub- 
sequently (see Figure 3). 

Critical periods may be regarded as those definable times dur- 
ing development when the organism is dependent upon environ- 
mental influences for its development to continue normally. Such 
experiential dependence at one critical period may represent an 
epigenetic crisis (Fox, 1970b; King, 1968), the onset and duration of 



Structure — ^Function 

Figure 3 . Highly simplified schema of various 
Hon where Jvironmental influences (E) may or 
determining influence, as exemplified by '"^7 

lions in domesticated animals. A, environmen a t ^ ..fired" dis- 
resistant development, e.g., of barking in dogs J r. recurs 
plays. B, environmental 

during a critical period, . ofdZelopment may be 

such as for song in some birds. C, direc J normal 

modified by input during a cLly handling 

maturation is not dependent upon this input) e g . ^ 

stress. D, varying environmental tnpuUunng considerable 

may influence maturation in many dirK . 
phenodeviance from the norm. (From ox, i9 


THE dog: its domestication and behavior 

the period being species-characteristic and therefore genetically 
programmed. There may also be interdependence between critical 
periods, where one critical period has an induction effect on a 
later period. One example of such delayed effects between experi- 
ences during an early critical period and a period later in life, when 
behavior is activated and is influenced by experiences during the 
critical period earlier in life, is the development of song in certain 
birds (Nottebohm, 1970). Another example is the early critical 
period for primary socialization which subsequently influences the 
development of secondary social relationships (Scott, 1962). 

Sensitive periods differ from critical periods in that the or- 
ganism is not dependent upon stimulation during such periods for 
development to proceed normally. It is rather that at particular 
periods in development the organism is especially vulnerable to 
certain environmental influences (temperature changes, elec- 
troshock, and experimental hormone manipulations) (Morton, 
1968) which may have profound effects on subsequent develop- 
ment. Experimental manipulations during such sensitive periods 
therefore may influence the integration of component parts of a 
particular system, e.g., adrenal or gonadal-hypophyseal axis 
(Levine and Mullins, 1966), and have long-lasting effects which can 
be detected later in life. 

In summary, therefore, critical periods may be regarded as 
those times in early life when the organism is developmentally 
dependent upon certain exogenous stimuli which are normally 
present in its sodoenvironmental milieu. Sensitive periods, in con- 
trast, are those times when the organism is especially vulnerable to 
environmental changes (change in temperature, maternal depriva- 
tion), the consequences of which are long-lasting. 

The developing organismic system is a link in the intrinsic 
complexity of interrelated systems extending in two dimensions; 
one in time, between ancestors'and future generations and the 
other, in space or place — the organismic system within a complex 
of ecological and social systems. The investigator may qualitatively 
catalogue, quantify, and dissect development at one of two levels, 
at the level of the process itself, or at the level of the interrelation- 
ships between processes or systems. Eventually he must reconsti- 
tute reality; that is, he must describe the developing organism in 
relation to its environment. Then developmental changes in terms 

Stages and Periods in Development 


of geneticaUy programmed, ecologically tuned or adaptive expec- 
idenMed”^ human-induced changes via domestication may be 

The potential environmental influences (as distinct from gene- 
fac selection per se), subsumed under the general phenomenon 
designated loosely as domestication, which may greatly alter a 
^ven spedes over successive generations are reviewed in this 
apter. Early handling stress (or prenatal gentling), imprinting 
and sodalization, and environmental enrichment (or deprivation) 
during sensitive and critical periods in early life represent the de- 
velopmentaUy timed stages when appropriate input may dramati- 
cally influence development and later behavior. This is illustrated 
schematically in Figure 4 and represents the three key interfaces 

Developing and Integrating Nervous System 



THE dog: its domestication and behavior 

between the developing organism and its environment where 
human domesticating interventions may have their greatest effect. 

Emotional reactivity is reflected in autonomic changes in car- 
diac activity. This most sensitive indicator has been utilized in a 
series of studies to evaluate some of the variables (such as the 
effects of early handling stress) discussed in this chapter. A major 
consequence of selection for docility in animal domestication may 
influence autonomic "tuning" and such possibilities will be inves- 
tigated in Chapter 10. 


Development, and 
Psychopathology of 
Cardiac Activity in the 


Weber and Weber (1845) first demonstrated that ^ 

vagal nerve causes cardiac inhibiHon. More 
(1958) reported that after cutKng the vagal neree, t P P 
rate in dogs was almost doubled due to the absence of ^ agal mh.b. 

‘‘“"-Belldn (r968) showed that 

portant behavioral mechanism m ma y , npctijnn birds, 

strated bradycardia Jo^haVre -r dr-ta.led 

stud^' M ■t^t- W 3yc”^a-'^fiuring sudde^-rnfi protonr4;fi 

immobility in roderits. Vanous reaction, rather 

were recorded, and in one spc« • ‘ (,^5-) observed fatal 

than tonic immobility, "•‘■'5 p.irasvmpalhetic system, 

cardiac arrest apparently mediate^ b) the p^ar. . „ P,„,„„. 
in wild Norway rats handled and I 


THE dog: its domestication and behavior 

Bradycardia is also seen in the diving reflex in many diving 
birds, in seals, and in man (Scholander et ah, 1942). Gellhom, in 
elaborating a useful theory on autonomic tuning of the central 
nervous system, observes that 

The immersion of the face in cold water leads to a vagal reflex 
which increases the resistance of the organism to asphyxia and 
is therefore of great biological importance in diving animals. 
Studies on this reflex in man with recordings of blood pres- 
sure, heart rate, oxygen saturation and skin temperature dis- 
close that the immersion evokes an immediate slowing of the 
heart rate which persists throughout the test. A rise in blood 
pressure and cutaneous vasoconstriction appear after the 
bradycardia. This reflex is therefore an example of a (parasym- 
pathetic) trophotropic reaction followed by compensatory er- 
gotropic (sympathetic) phenomena. If the immersion test is 
carried out on an "apprehensive" subject the vagal reflex is 
greatly increased, illustrating the enhanced trophotrophic reac- 
tivity in a trophotropically tuned subject. Contrariwise, harass- 
ing the subject, a procedure known to induce a state of ergo- 
tropic tuning, may delay or abolish the immersion reflex, thus 
exemplifying reciprocal inhibition of the trophotropic system in 
this state. 

Other aspects of Gellhorn's theory are discussed subsequently, 
relevant to the central issue of the study in this chapter. (Gellhom, 

Sudden fear in man may evoke bradycardia which may be* 
followed by fainting (Engel, 1950) or even sudden death (Wolf, 

The excellent review of Fara and Catlett's (1971) study of car- 
diac responses and social behavior in guinea pigs provides a basis 
for exploring further behavior-related cardiac phenomena in 
mammals. Adams et ah (1968) have recorded marked bradycardia 
in cats prior to responding to attack by a conspecific. 

There may, however, be enormous species and individual dif- 
ferences. A normal dog, socialized to people, will show a marked 
bradycardia when handled by a person, in contrast to the 
tachycardia reported lor the guinea pig by Fara and Catlett (1971). 
Does this imply that some species have more or less vagal or sym- 

Behavior, Development, & Psychopathology of Cardiac Activity 179 

pathetic tone than others? Also, what effects might domestication, 
early handling stress (Denenberg, 1967), socialization (Scott and 
Fuller, 1965), or the lack of socialization in the dog have on such 
cardiac responses. 

Heart rate is, to date, the most accessible, if not the most 
accurate, measure of changes in autonomic activity — constituting a 
quantifiable physiological measure underlying emotional re- 
sponses in various social contexts. 

Lacey and Lacey (1970) present additional data on the 
bradycardia phenomenon in man, as well as some startling, if not 
controversial, conclusions. Transient bradycardia is regularly re- 
corded during orientation and attention. Those tasks requiring 
only simple environmental reception produce significant cardiac 
deceleration, while difficult tasks, entaiUng internal cogniHve elab- 
oration of a problem-solving sort or requiring exposure to noxious 
stimuU, produce massive cardiac acceleration. An activation re- 
sponse (getting ready to respond to a conditioned signal), an an- 
ticipatory cardiac deceleration, also occurs, which is an indicator 
here of high motivation. . 

Israel (cited in Lacey and Lacey, 1970) has identified an 
ing relationship between this bradycardia of a en on a 
"cognitive style" of an individual. So-called sharpeners pay at en- 
tion to everything, focus on differences rat er an s‘ ' ‘ ' 

and habituate slowly (a description that would h' ^ 

canids). Other human subjects belonged 

who tend to make global judgments, habitua ^ ^ .jij;,), 

inattentive to many details of the environment^ desmpt on « h ch 
partially fits the average domesticated dog). The l^velers sho«^a 
lesser attention bradycardia than the sharpener . demon- 

of this study is not the analogy with canids, but rather he demon 
Station that physiological iabiUty parallels the ° attitude 

manifest overtly toward the external envronmen . Centi^^ nert o^us 
system activity and behavior <'"''[^‘*'"^j|f,'"f^"greater‘conlrol of 
tive style), therefore, appear 'n supposed bv ive.stem 

autonomic activity than was hith PP rccocnized 

psychophysiologists, although this fac “ 8 Kurtsin's 

fho^ugh'^no^ qua^ntified by PaHowan <-^:;:,:u,on- 

1968 overview of co^tlCo^^scc^aI ana 


THE dog: its domestication and behavior 

Lacey and Lacey (1970) go on to show that this cardio- 
deceleratory response is correlated with Grey Walter's DC shift 
in the EEG activity— the contingent negative variation (CNV) 
which reflects the organism's readiness to respond. Apparently, 
the greater the CNV, the greater the cardiac deceleration. 

The question now arises as to which comes first. Research by 
Bonvallet et al. and Zanchetticf al. (cited in Lacey and Lacey, 1970) 
shows conclusively that cardiovascular afferent input to the CNS 
results in a change in CNS activity. For example, elimination of 
glossopharyngeal and vagal input (to the bulbar inhibitory area) 
leads to poststimulation cortical activation. Thus viscerocortical af- 
ferents have an inhibitory effect on the CNS. 

Lacey and Lacey (1970) conclude that 

The temporary hypertension and tachycardia observable in 
acute emotional states and in "aroused" behaviors of all sorts 
may not be the direct index of so-caUed "arousal" or "activa- 
tion" they are so often considered to be. Instead they may be 
a sign of the attempt of the organism instrumentally to con- 
strain, to limit, and to terminate the turmoil produced inside the 
body by appropriate stimulating circumstances. Moreover, to 
quote from an earlier statement of ours, 

... if increases in blood pressure and heart rate signal a 
physiological attempt to restrain excitatory processes, then it 
seems likely that their diminution, absence, or conversion to 
blood pressure and heart rate decrease signify an absence of 
this restraining process and, therefore, a net increase in excita- 
tion; a lowering of threshold, a prolongation of the impact of 
stimuli, an increase in spontaneous activity, and the like. 

It is this last interpretation, and derivatives from it, that ap- 
pealed to us as indicating the most strategic and dramatic ap- 
proach to demonstrating the role of cardiovascular activity in 
the behavior of intact humans, and to challenging current acti- 
vation theory, which has long seemed to us to be a grossly 
oversimplified view of the role of autonomic and skeletal activ- 
ity in behavior. 

(They cite research by Bonvallet et al. showing that distension of 
the carotid sinuses could cause a dog or cat electrocorticogram to 

Behavior, Development, & Psychopathology of Cardiac Activity i8i 

appear as though the animal were sleeping.) Thus^ the possibility 
arises that increases in blood pressure and heart rate may be 
physiological attempts to restrain excitatory processes rather than 
serve as a direct index of arousal or activation. Their logical deduc- 
tion of the reverse is that decreased blood pressure and heart rate 
signify an absence of this restraining mechanism, a net increase in 
excitation, and a prolongation of the impact of stimuli. 

Graham and CUfton (1966) have come, independently, to a 
similar conclusion vis that an increase in heart rate and an increase 
in blood pressure lead to inhibition of cortical activity and would 
presumably be associated with reduction in sensitivity to stimula- 
tion (as in defensive-protective reaction). Conversely, they 
theorized, heart rate decreases should be associated with increase 
sensitivity to stimulation (as in orientation or taking in t e envi 


Lacey and Lacey (1970) also observe that: 

We are doing chronic animal studies now 1 *^ ^ 

strate that thl visceral afferent tal S 

operate in the way we think it does, in ® solved 

tions we have described. Many problems 

and much work done before really effective demonstrations 

can be made. 

In the meantime, the cardiovascular 

psychiatricstudy, notasanonspea cmdexo 

tion, but as a h|ghly_speafic ^d appare y 
sponse mechanism, integrated at and revealing 

affechve and cognitive variaHons P P' ^ j^al ivith 

specific personal idiosyncrasies in the way p P j 

their external world. (Lacey and Lacey, i 97 - PP- 

Sodaliialion of the dog to f"'’" (ho 

tachycardia. It was only later that u > ^ ^ dramatic 

ining and auscultating the dog was the cause 
cardiac phenomenon. nee of a human tvmg 

Pavlov (1928) obsen'ed that P , fp^pnnse. so he h.ul lo 
could easily inhibit an ongoing conditioned respon 

i 82 

the dog: its domestication and behavior 

isolate his animals for study. Later he found that specific responses 
were evoked by certain people, and he postulated the existence of a 
social reflex in the dog. 

Research on the involvement of the autonomic nervous system 
in behavior and in the establishment of conditioned reflexes and 
experimental neuroses in dogs was made possible with the advent 
of electronic physiological monitoring in the early 1940s. Gantt 
(1944), a student of Pavlov, was the first to demonstrate that the 
autonomic nervous system was easily influenced by the presence 
or absence of human contact, even when no overt behavior was 
manifest. One psychotic dog with catatonic symptoms, had a nor- 
mal resting heart rate of 200 beats/min, but in the presence of a 
human being it would fall to 12 beats/min. Cardiac arrest, some- 
times for as long as 8 sec, was recorded in this dog when in the 
presence of a person (in spite of which it lived for 14 years in the 
laboratory) (Newton and Gantt, 1968). 

Subsequent research by Gantt ei al. (1966) demonstrated car- 
diac changes in the rabbit, cat, dog, guinea pig, opossum, and 
monkey caused by the presence of people. Two consistent observa- 
tions were reported in the dog; an increase of 10-80 beats/min when 
a person entered the room where the animal was and a decrease of 
5-40 beats/min .when petted. 

Royer and Gantt (1961) subsequently showed that the cardiac 
response to petting in the dog was not an automatic reflex reaction. 
Several dogs would only show petting bradycardia with a familiar 
handler; a stranger evoked no response or sometimes tachycardia. 
Familiarity with the person is therefore of major importance. Scott 
and Fuller (1965) noted that there were differences among breeds in 
response to a person entering the experimental room, bradycardia 
being seen in cocker spaniels and tachycardia especially in basen- 
jis. The former breed, especially selected for passivity and crouch- 
ing, may be demonstrating a response comparable to fear bradycar- 
dia (see discussion later). 

In a very original series of experiments. Lynch (1970) demon- 
strated that the bradycardia evoked by petting in dogs was not a 
simple reflex but was rather an integral component of an emotional 
reaction toward the person. He showed that tactile contact has a 
potent effect on the cardiovascular system of dogs to the extent that 
fear or pain (shock-induced) responses may be blocked, and the 
usual tachycardia to such conditioned stimuli was inhibited. 

Behavior, Development, & Psychopathology of Cardiac Activity 183 

It has long been known that “contact comfort" of a hurt child 
(or pet animal) by the parent (or owner) "makes the pain go away." 
Lynch (1970) presents physiological evidence in support of this 
objectively unlikely phenomenon. The quieting effect of the pres- 
ence of handler or familiar keeper in many species of domestic and 
wild captive animals is explained by these findings as is perhaps 
the potency of reward to a dog in a mere stroke from its master. 

Unfortunately, neither Gantt nor Lynch considered the 
paradox of bradycardia evoked by contact in dogs that were afraid 
of people or unsocialized (feral) and the bradycardia they demon- 
strated in socialized dogs that were friendly toward people. A 
twitch on a horse or muzzle on a dog may evoke a comparable 
calming effect as does the presence of a handler m more tractable 
animals. The physiology of restraint and potenHally harmful con- 
sequences of excessive autonomic reaction to enforced restraint or 
tonic immobiUty induced by pain or fear warrant further study. 
Furthermore, genetic influences (selection for domes ca on 
addition to such early experience variables (soaalizahon to man) 
have not been studied, hence the emphasis m this smdy on wild 
(undomesticated) canids and unsodalized (feral) coyote x dog hy 

'’"‘^Contact comfort evokes a clear 
reflected in bradycardia). A dog will work in or er 8 
reward from its Lndler; petting a dog ° 

pain or react fearfuUy to a condiHoned „ 

thetic arousal and tachycardia. What role might phen^rncno^ 
have in development and in establishing soaa 
man and animal? , fVm to- 

Lynch (1970) reports ,2 and 16 weeks of 

sponse to petting develops nod for soanliz,ition 

age in the dog, somehme ‘Tfound that the presence of a 

(which is from 4-12 weeks ot age). H I rale in a 

person (without contact) caused a 40 ,0 , Liddell (1954) 

distressed and socially isolated P“PP>', "■'^;|:^'3Vul^n:a mnin’en. 
found that if a kid or Iamb was expos .m resist the stress, 

in the presence of its mother, it cou Mother succumK'd 

sibling hvins stressed in the ab^n dis,urKinci-s into 

rapidly, and some showed persislcn 

maturity. the lack of tactual 

Thus, the question now anscs concerning me 


THE dog: its domestication and behavior 

contact on behavioral development, on the establishment of social 
bonds, and on subsequent resistance to stress. 

Contact (petting or maternal care) would seem to facilitate the 
attachment or socialization process. Deprivation may cause severe 
and long-lasting behavioral and physiological changes in man and 
other primates (Harlow, 1959; Bowlby, 1953; Spitz, 1950). Tactile 
contact appears to be physiologically and psychologically beneficial 
(if not essential) for normal development. A dependence upon 
parasympathetic stimulation (evoked by the mother or handler) 
may also facilitate socialization. In the absence of such other- 
directed stimulation, isolated animals (puppies and infant rhesus 
and human infants) will effect self-stimulation (tail- or thumb- 
sucking, self-clutching, and rocking). The need for such stimula- 
tion in immature organisms may be important for the maintenance 
of normal physiological homeostasis. Without it, development is 
impaired. Also, if deprived of contact, stressful stimuli may not be 
adaptively countered by a parasympathetic reaction (as demon- 
strated by petting bradycardia [Lynch, 1970]). Stress factors (such 
as hospitalization) may then be intensified. Therefore, this is of 
considerable clinical significance in veterinary medicine and 
human pediatrics. It is also relevant to the husbandry of farm ani- 
mals where stresses associated with transportation, weaning, and 
maternal separation are major causes of livestock losses and im- 
paired growth. 

Experiment I. 

Development of Heart Rate 

The heart rates for four breeds of dog (beagle, wirehaired fox ter- 
rier, Shetland sheep dog, and basenji) were recorded at weekly 
intervals from 1 to 5 weeks of age. Data from ten subjects of each 
breed were then averaged to give an overall view of rate changes 
with increasing age. Individual and breed differences were not 
analyzed (see later), since the purpose was simply to collect data 
representative of a heterogenous, pooled sample. 

Behavior, Development, & Psifchopathology of Cardiac Activity 185 

Subjects were held in the experimenter's arms and the heart 
rate measured using a stopwatch and stethoscope. 

From an average rate of 220 beats/min at i week of age, there 
was a rapid decKne to 192 beats/min by 3 weeks. After this age, the 
resting heart rate gradually increased to an average rate of 208 
beats/min at 5 weeks. (See Figure i.) 

Suspecting that this developmental pattern was due to a 
gradual increase in vagal inhibition, data were collected from sev 
eral mongrel and beagle dogs from birth to maturity ? 

age), following injection (IM) of atropine sulphate (0.5 mg/ g). is 


THE dog; its domestication and behavior 

would, by selectively blocking the vagal effect on cardiac activity, 
reveal at what age vagal inhibition begins to develop. 

Interestingly, and as predicted, there was no significant in- 
crease in heart rate until after lo days of age. The greatest release 
from inhibition occurred between 2 and 3 weeks of age, which 
tends to support the contention that the initial postnatal decrease 
in heart rate is related to the development of vagal inhibition. 

The more gradual increase in heart rate following atropiniza- 
tion from 1 month of age through to maturity suggests that in 
addition to the relatively abrupt onset of vagal modulation of car- 
diac activity, there is also a more gradual increase in vagal tone. 
(See Figure 2a.) This latter phenomenon is to be anticipated in a 
species such as the dog, which is characterized in maturity by a 
high vagal tone compared to other species such as the rabbit, which 
have a greater sympathetic tone. Additional cardiac phenomena in 
young caruds are shown in Figures 2b and c. 


Figure 2a. Ontogeny 0/ olropine effect on dog heart. 


Behavior, Development, & Psychopathology of Cardiac Activity 187 


Figure zb. Various treatment effects on heart rate in normal and 
fading 2-day-old puppies: pronounced bradycardia in the latter. 
(From Fox, 1966.) 


Using direct auscultation and biotelemetric monilonn^ heart rale 
development was recorded from birth unHI 8 'veeks of age m five 
beagles, six coyotes, and three F3 coyote x beag e y n s. n a 
subjects, the previously described rate decrease between 2 and 3 
weeks of age was confirmed as a developmcnla p cnomcnon in 

dependent of handling (petting or human contact). 

Petting per se did not evoke a significant bradycardia until 
around 5-6 weeks of age; this effect rvas transient b'to m 
contrast to the more sustained bradycardia recor e i . - • 

Subjects with high resting heart rates "f. 
postnatally could be identified later as being the most active and 



I00»»I , 


Figure 2C. Periods of apnoea during various states of sleep are 
often accompanied by changes in heart rale. 

outgoing canids. Others with lower heart rates tended to be more 
passive or timid later in life. 

This latter observation compares well with Scott and Fuller's 
(1965) developmental study of breed differences in heart rate. They 
found that the most outgoing breeds, wirehaired fox terriers and 
basenjiS/ had overall higher heart rates than the more passive shel- 

Behavior, Development, & Psychopathology of Cardiac Activity 189 

ties, beagles, and cocker spaniels. While the fox terriers were con- 
sistently different from 2 weeks of age, the other breeds did not 
individuate until after 7-8 weeks of age. 

Lockwood (personal communication), working in my labora- 
tory, concluded that the initial contact bradycardia of short duration 
in very young canids may be analogous to an orienting response 
(see also Lacey and Lacey, 1970). He also recorded a transi- 
ent bradycardia when contact with a neonatal canid was broken; 
this “off response" may be an important autonomic indicator re- 
lated to behavioral regulation of homeostasis, i.e., contact with 
mother for thermoregulation and nurturance must be maintained. 

Confirming the findings of Scott and Fuller (1965), it was 
found that heart rate and sinus arrhythmia are highly interdepen- 
dent in older canids. A slow heart rate (i.e., high vagal tone) is 
arrhythmic, and conversely, a high rate is regular without any 
arrhythmic inclusions. Scott and Fuller (3965) demonstrated breed 
(genetic) differences in these interdependent physiological indi- 
cators of autonomic activity and emotionality. It will be demon- 
strated shortly how early experience (handling stress) may also 
influence cardiac activity in later life. 

Experiment 11. Can Early 
Experience Influence Cardiac 

Research on early handling stress in rodents (Denenberg, 1967; 
Levine and Mullins, 1966) has shown that the adrenal-pituitaiy 
axis can be affected so that reactions to physical or emotional stress 
are more graded and adaptive than in control animals. The latter, 
unstressed in infancy, tend to overreact to stress. Early handling in 
rodents also enhances learning ability under stressful conditions, 
since emotional arousal is loss than in controls and so does not 
interfere with performance. Resistance to cold exposure, starva- 
tion, implanted neoplasms, and wal leukemia has also been 
shown to be greater in rodents subjected to optimal handling stre^^s 
in early life. Even more remarkable is that this phenotvpic 


THE dog: its domestication and behavior 

modification is transmitted nongenetically over several generations 
(Denenbetg and Rosenberg, 1967) and may be instigated prenatally 
by handling the pregnant mother (Joffe, 1969). 

The findings imply that environmental influences (i.e., stress) 
during a critical period in early life have profound and enduring 
consequences and may well influence sympathetic-parasympa- 
thetic tone as well as determine emotional reactivity or tempera- 
ment in later life. 

Blizard (1971) has discussed the significance and possible clini- 
cal implications of individual differences in autononaic responsive- 
ness (cardiac activity) in laboratory rats. He found that rats given 
handling stress from 1-7 days of age exhibited dimiiushed cardiac 
response to handling and to novel stimuli in adulthood compared 
to nonstressed controls exposed to these stressors for the first time 
as adults. Environmental influences early in life, therefore, have a 
clear effect on emotionality and, because of the reported influence 
on heart rate, may enhance trophotropic or parasympathetic tone 
in laboratory rats. 

Theoretically, at least, the autonomic-neuroendocrine interre- 
lationships and temperament per se may be similarly modified in 
the dog. The potentials for such phenotyq>ic engineering may also 
have considerable practical value in raising dogs for stress resis- 
tance, an important consideration for military and peace-force use. 

Given, then, that vagal tone is not already established at birth 
in the dog, it might be possible to modify sympathetic or parasym- 
pathetic tone by enhancing the former via handling in early life, as 
demonstrated in the aforementioned studies with laboratory 10= 

Therefore, it was decided to evaluate the physiological and 
behavioral effects of early handling in domesticated dogs. Four 
litters of random-bred pups were used, half of each litter being 
used as nonhandled controls (eight in all) and the remaining eight 
pups subjected to the following regjme from birth until 5 weeks of 


This experiment was designed to determine the effects of differen- 
tial rearing on several aspects of behavior and development of the 

Behavior, Development, & Psychopathology of Cardiac Activity 191 

dog. Sixteen dogs were studied (eight control, eight handled). The 
handling procedure and behavioral tests are described in Appen- 
dix I. 


No significant difference in body weight gain was observed in the 
groups, nor were significant differences in organ weights or in total 
brain weight observed. When subjects were tested at 3 and 4 weeks 
of age by a variety of neurological responses (Fox, 1964), no signifi- 
cant differences were observed. Some handled pups, however, 
showed slightly superior coordination while standing and walking 
at 4 weeks. Histological examination of motor, occipital, and fron- 
tal cortex and vestibular neurons revealed inconsistent differences 
in neuronal size, but no differences in cell density were observed. 
Vestibular neurons in four handled subjects were significantly 
larger and contained more chromatin than those in the control or 
isolated pups; the total population of neurons observed in senal 
sections contained fewer small-sized neurons. The Meynert cells of 
the fifth layer in the occipital cortex and those of the fifth layer in 
the frontal and auditory cortices (large pyramidals) appeared larger 
in three handled pups compared with Uttermate controls, and they 
contained more Nissl substance. Heart rates were recorded in the 
control and handled groups at weekly intervals 
at 5 weeks of age with surface electrodes, at which tune su^ects 
were not handled (see Figure 3). Tlie marked 

the handled and control groups were apparent from the second 
week onward. Normally there is a decrease in heart 


found to be 63% ± 7 m the contro . Hlinc^ but there was a 

total amino content of the adrenals due 1 ende con- 

significant increase in epinephnne. n in g 

tent of the kidney and adrenals controls, which 

found in the handled pups compared with their 


the dog: its domestication and behavior 




ERG— 4444444444444^ 

so pvl I 



Figure 3. Sleeping EEG of handled and control g-week-old pups. 
Note greater maturity of EEG of handled pup (higher amplitude) 
and also faster resting heart rate. 

may indicate an increase or change in lipid metabolism as a result 
of early handling. 


Extreme differences were not found among individuals in the same 
group, and this surprising uniformity facilitated comparisons be- 
tween the two differentially reared groups. These data have been 
summarized in Table 1. Generally, the handled pups were hyperac- 
tive, highly exploratory, very sociable toward humans, and domi- 
nant in social situations (e.g., play) with their peers. The handled 
subjects showed the greatest distress vocalization immediately after 
the handler had entered the testing arena and removed the cloth 
and toy. In contrast, the control subjects were little distressed by 
this interference but showed great emotional arousal when first put 
into the arena. In the barrier test situation, the handled pups per- 
formed best in that they requited fewer trials to negotiate the dc- 

Table I. 

Behavior, Development, & Psychopathology of Cardiac Activity 193 


THE dog; its domestication and behavior 

tour, whereas the control pups reacted more slowly and showed 
distress vocalization in this situation (Table I). In the control group, 
therefore, emotional arousal in this situation prejudiced problem- 
solving ability. 

Recordings of EEG of all the handled pups showed a greater 
amplitude during light sleep than those of the control subjects 
(Figure 4). As amplitude increases with age, it may be presumed to 
be an indication of greater maturity in the handled subjects. No 
difference in amplitude or fast frequency components were ob- 
served between the handled and the control pups in the alert state. 
A similar observation has been made on EEG maturation in kittens 
following early handling (Meier, 1961). 

From these findings a pilot project was set up in cooperation 
with the Biosensor Research Project, U.S. Army Veterinary Corps. 
Several litters of German shepherd pups were given the early han- 
dling stress from birth to 4 weeks of age, each subject receiving 
only 1 min on a 45 rpm teeter-totter that gave both lateral and 
angular vestibular stimulation and i min cold exposure at 37°F. 

Rgun.- .(. Hart ralfS of conitol and handled dags. Stale sustained 
higher hcnrt rales in handled pups. 

Behavior, Development, & Psychopathology of Cardiac Activity 195 

Prelimmary results so far are extremely promising. As adults, such 
dogs have reportedly superior stamina under conditions of heat 
stress in the tropics. Data on disease resistance and longevity are 
not yet available. But a word of caution should be added. As 
Ginsburg (1968) has shown, working with different inbred strains 
of mice, the same handling stress may vaiy from one strain to 
another — having no demonstrable effect in some, enhancing oth- 
ers' later stress resistance, or lowering stress resistance in others. 
In a more heterogenous dog population, therefore, early handling 
may produce comparable results; thus, the quality and quantity of 
stress must be carefully regulated on an individual basis. Ideally, a 
suboptimal handling regime should be instigated (e.g., i min 
teeter-totter stimulation followed by 1 min gentle stroking, then 1 
min cold exposure followed again by 1 min gentle stroking). 

Under natural conditions, a wild canid mother may leave the 
cubs for extended periods, and they would be exposed normally to 
more stresses in early life than the relatively overswaddled home- 
raised litter. 

Several breeders over the past 2 years have set up a simple 
handling stress regime using half of each litter, the other half being 
controls. Based upon subjective reports, all are enthusiastic and 
believe that this method of phenotype enhancement Is a valid phe- 
nomenon (which controlled laboratory research has already dem- 
onstrated!) and a valuable addition to the usual rearing practices. 

In fact, there is less originality in the application of this phe- 
nomenon in improving the temperament of domesticated animals. 

As Denenberg and Whimbey (1963) have suggested, prenatal han- 
dling or gentling of the pregnant mother and early postnatal han- 
dling of the offspring were probably practiced unwittingly as a part 
of animal husbandry early on in the domestication of both farm 
and pet animals. 

The marked difference in the age-related changes in heart rate 
in the four breeds of dog described earlier and the control subjects 
in this latter study warrant scrutiny and explanation. The controls 
received regular daily contact with people and were well sodalizcd 
and more used to being handled than the pups of four different 
breeds that were handled only at weekly intervals for recording 
growth and heart rales. The increase in heart rate in these dogs 
after 3 weeks of age (at the beginning of the critical period of 


THE dog: its domestication and behavior 

10 sec 

Petting Bradycardia ^ Dog 

Figure 5. Petting bradycardia in a female dog. 

socialization) may be a reaction to being restrained and handled. 
Such tachycardia, indicative of flight or emotional arousal (fear), 
has been recorded in several dogs of various ages. In socialized 
canids, however, a slowing of the heart rate occurs (see Figure 5). 
This contact bradycardia is discussed subsequently. It should be 
emphasized that the tachycardia that developed in the handled 
pups after 2 weeks of age was not correlated with fear or other 
emotional disturbance. On the contrary, these "super-socialized" 
puppies never resisted restraint or handling. Most significantly, 
they also manifested tachycardia even when resting unrestrained, 
with EKG being recorded by surface electrodes rather than by 
stethoscope (see Figure 4). 

Clearly, such variables as socialization, habituation to han- 
dling, restraint and the method of measuring heart rate (either with 
surface electrodes to a polygraph or.via stethoscope) are significant. 
Subsequently, therefore, heart rates were recorded with a bio- 
telemetry transmitter directly through a receiver onto a physio- 

Experiment III. 

Individual Differences in 
Heart Rate and Temperament 

Tile next question was to follow up the marked effects of early 
handling on cardiac activity and behavior (i.e., phenotype 
modification) with a study of individual differences within litters of 
canids given no handling stress. Individual differences in heart 

Behavior, Development, & Psychopathologi/ of Cardiac Activity 197 

rate, if present, may correlate with other measures of emotionality 
and behavior and be an indicator of autonomic tuning or sympa- 
thetic tone independent of environmental (stress) influences; such 
individual differences, which can be created by handling stress, 
may also be genetically predetermined as part of a young animal's 
basic psychophysiological constitution or temperament. 

If such individual differences could be demonstrated, how en- 
during might they be and how, under natural conditions, could 
they influence disease resistance, fertility, and other eventualities 
demanding adaptation to some form of stress? 

Also, if there is consistency in such individual differences in 
heart rate and a high correlation of this measure of autonomic 
activity with other measures (of behavior, emotional reactivity, 
and learning abiUty), we may have an extremely sensiHve index or 
test protocol for puppy evaluation. Such early evaluation has ^eat 
applicability for screening litters of puppies and selecting in lyi u 
als at an early age for special rearing and training programs (e.g., 
military dogs, guides for the blind, etc.). 

This possibiUty has been explored from a somewhat differenl 
perspective in man. Thomas el al. (197°) devise a ° 

tests to evaluate the emoHonai/autonomic 
neonates. From these measures, they were ® ^ ° ament would 

predictions as to what the later personality or . ^dv the 

he-, these predicHons were verified in th.s 

subjects now in their late teens. From a prac ” ^ . ^^^jd 

relative to dog and man, such early ^ jp order 

« one to In.lijele ,h„ 

emotional disturbance following change m rou 
of immediate reward or comfort). . , caotive adult 

An initial pilot study -- 

wolves at the Naval Arctic Rere ^ b.otelcmeters 

Alaska. Working in collaboration I ^ yearling wolves, the 

were implanted bers of adaptive pack being 

highest- and lowest-ranking m j ^g hr to monitor 

selected. Recordings were '^ben 

possible circadian vanables m ac > highest-ranking wolf 

and overall motor acliv'ily was grea 

THE dog: its domestication and behavior 


It was tentatively proposed (Fox, Folk and Folk, 1970) that such 
marked physiological differences might be predetermining factors 
for temperament and social rank. 

With these promising findings, the following experiment was 
designed to explore further the possible significance of individual 
differences in heart rate correlated with other behavioral measures 
in unsodalized 6 to 8-week-old wolf cubs. This species was chosen 
in order to rule out any potential anomaly in vagal tone which, in a 
domesticated species, together with socialization effects, might 
have a significant influence on cardiac activity. 

In the present investigation, a temperament or reactivity pro- 
file was made for each cub in two captive litters (as detailed by Fox, 
1 ^ 97 ^)/ and the social rank of each cub was ascertained. Cubs of 
high, low, and intermediate scores were then selected for 
biotelemetric monitoring of heart rate under various test condi- 
tions; some of these subjects were then used in a stress study, the 
response being determined by changes in plasma cortisol levels 
over time. 


Twelve woiS cubs from two litters were studied between 6 and 8 
weeks of age. A series of tests, described in detail in a recent study 
of individual differences in behavior of wolf cubs (Fox, 1972), were 
run (see Appendix II). 


The scores for group and individual prey-killing, dominance (aver- 
aged scores from repeated tests), and the reactions to the novel 
stimulus are detailed in Table II. The close correlations between 
social rank, prey-killing, and exploratory behavior, as demon- 
strated earlier (Fox, 1972) are clearly evident in these two litters. In 
this earlier study, the question of social facilitation versus prior 
experience was posed since the group prey-killing test was con- 
ducted after the individual tests. The data in Table 11 show that 
social fadlitation may indeed be present in the group test and 

Behavior, Development, & Psychopathology of Cardiac Activity 

Table H. 


Group Individual Exploratory 

prey-killing prey-killing Dominance behavior 

Litter I 

ScBl 6^ 5 

BI 5 

ScBr 6 4 

RcBl 9^ 4 

UcBr 9 4 

CCBr d 4 

CCBr 9 4 

KcBr d* 4 





















Lii/CT- II 

ScBl 2 3 

RcBl 62 1 

BlUc 9“ 1 0 

CCBl d" 0 0 

•Selected for EKG and corticosteroid stress studies. 

would account for the high scores of 

tested alone later, despite prior expe^nce, low sco^Dd 
ferences in the magnitude of scores behveen ^ , 

marked. In the earlier study O^ox, ’97=)' 
produced a similar outgoing litter the pr • ^ 

lowest scoring litter in this ' ' 

dam to Utter II (both being sired by pmeedur.-s 

Changes in heart the vanous h^ndh^^^^^ 

aregraphically represented m F^ 6 ^nuct and 

finding was the bradycardia assoa^ r - 

Heart rote /mm 


THE dog: its domestication and behavior 

orma; j. b 4. canlacis the aib; 5. obfcrvcr Imb off; 6. cub is picked 
up and held; 7. cub is ieft in arena and baseline rale recorded 8 
ol^rrer makes eye contact; 9. baseline rate recorded; 10. response 
to suddai noise. 

passive submission (or freezing). A second consistency was the 
lugher baseline heart rates in the dominant cubs over the subordi- 
nates, a consistent:)' which adds to the obsers'ations of Fox et al. 
(1970) who reported a higher heart rate over a 24-hr circadian 
periodicity study of a dominant yearling in contrast to its subordi- 
nate littermate. Bradycardia also occurred when the cubs were 
picked up. A less marked bradycardia was recorded when the ex- 
perimenter rem.ained passive in one comer of the arena and also 
when eye contact alone was made around the .screen without the 

Behavior, Development, & Psychopathology of Cardiac Activity 



experimenter being in the arena. In toth cubs. Tachycar- 

eye contact was most marked in the o recorded in RcBI ^ 

dia, instead of the anticipated g and 7 ), ihis reaction 

ofLitterlandCCBl d of Utter H (see Ft^res^=^^7; 

being correlated with defensive-aggro® those cubs ®o*’)ocle 
Changes in /xg% cortisol U tho p a .f^gnt trends (see a c 

to the stress experiment revealed som [,jrh arc quite capa c 

HI). Generally, the highest-ranking^' delay the re- 

of adrenal response (according to bccon. lo contrast, 

sponse for a time after the ^ 

of intermediate social rank resp<^ f further secretion 

of cortisol secretion and are capab eo in te 

treatment. Subordinate animals am n jtn.’S'^. oor do tht> 
increased levels of plasma cortiso ^ ACTM 

a capacity for adrenal secretory resp 


THE dog: its domestication AND BEHAVIOR 

Table III. 


Cortisol in plasma (fig%) 





5 min 

10 min 

30 min 

60 min 

Utter I 

a ScBl d 







/3B1 9 







e RcBl 9 







(i> KcBr d 







Utter II 

a ScBl 6 







€ BlUc 9 







u CCBl d 







Utter I 

a ScBl d 







to RcBr d 







Lillcr 1/ 

o ScBl d 







€ BIUc 9 







•Control, serial blood samples taken from time of confinement with no further 

‘ACnf. troated with ao lU Acthar (IM) at time of conrinement. 

It should be emphasized that the cubs of Utter II were more 
timid than most of those of Utter I (see Table II); in the responses of 
the dominant cubs of the two litters, for example, the dominant 
cub of Utter II resembled more a lower-ranking cub of Litter I. 

T^ese findings are discussed subsequently and correlated with 
individual differences in both cardiac responses and behavior ns 
demonstrated in the various tests described earlier. 

Behavior, Development, & Psychopathology of Cardiac Activity 203 


The behavioral test scores for prey-killing ability and exploratory 
behavior show a close correlation with rank scores for social domi- 
nance, especially in the more outgoing Litter 1. These findings 
support the earlier study of individual differences in wolf litters of 
Fox (1972). In this earlier study, the question of social facilitation of 
prey-killing arose and was not completely answered. The present 
study was in part designed to answer this question, by giving the 
test v\dth live prey to the whole litter prior to testing each indi- 
vidual. Several cubs had lower scores when tested alone with live 
prey than they had when tested with conspedfics. 

The long-term significance of these tests should also be em- 
phasized; cubs tested at 8 weeks could be identified ^ the basis of 
their scores when retested t year later (Fox, 1972^ This serves to 
highUght the notion that the temperament of each individual es- 
sentially is determined innately. Or, at least f e 
phenotype is formed by 8 weeks, so that by this age ear y exp 
ence has established a stable state (i.e., ' • 

teractions are stabilized by 8 weeks). This asic e P ' 

which may be a constellation of autonomic 
pathetic response threshold, and emotional 5"^' 

influences the way in which ivjih 

to prey, and to novel objects. Such expenence , critical 

a particular temperament constellation during hchivior at 

wLks of life, determine subsequent =°7'>'.”"Vwhh^^hrpack 
least up to the first year of life. Certain wUhm p^ick 

may confound such predictions where a -aj 

become a subordinate outsider with ma un y . hichcr rcst- 
A consistent finding in the heart h^h- 

ing heart rate, indicative characteristic of the 

ranking wolves, while '°'r''j2nKS support those of Fox el at 
most subordinate cubs. These fin g .PP ,j ,j, (in a arcadian 
(1970) who found a higher heart rate nd ac . 
analysis of cardiac activity) in dominant tn 

ling wolves. . nne parts of the test se- 

The marked bradycardia ma fn-ezine or passive im- 

quence with a handler is associated with fn-czang P 


THE dog: its domestication and behavior 

mobility and has been recorded in many vertebrates (Belkin, 1968), 
as well as in unsodalized F, coyote x beagle hybrids during han- 
dling (see later). This bradycardia is to be distinguished from pet- 
ting bradycardia in sodalized dogs (Lynch, 1967) and other canids 
(see later). The contact bradycardia is of much longer duration than 
the orienting and attention bradycardia described in man (Lacey 
and Lacey, 1970) and is to be differentiated from the bradycardia 
which occurs after stress-induced tachycardia as immediately fol- 
lowing a fight, for example (see later). 

Candland et al. (1970) have studied changes in heart rates in 
squirrel monkeys in various sodal contexts, notably during aggres- 
sion and establishment of dominant-subordinate relationships. 
They found that heart rate was related to rank on the status hierar- 
chy by a curvilinear function; middle-ranking animals showed the 
lowest heart rates during test sessions but not during baseline 
measures in the home cage. In chickens (Candland, et ah, 1969), 
they found a similar U-shaped function; alpha and omega birds 
showed the highest heart rates during intraspecific test sessions, 
and middle-ranking ones had the lowest rates. These authors ques- 
tion why animals of both high and low rank should show higher 
heart rates than middle-ranking animals. It is not inconceivable 
that those of low and high rank have a greater sympathetic arousal 
associated respectively with threat or readiness to attack and flight 
or defense. Those of middle rank may have a greater parasym- 
pathetic tone related to passive submission or passive avoidance of 
conflict, so that escape-assodaled tachycardia is not manifest as in 
subordinates, (i.e. Tachycardia may be related to fight and flight in 
high- and low-ranking individuals.) Marked tachycardia was re- 
corded in the squirrel monkeys during handling as distinct from 
the bradycardia of the wolf cubs. 

Candland et al. (1970) found that when an individual experi- 
enced a change in social rank, there would be a predictable change 
in heart rate which correlated with its new rank position. These 
findings would be interesting to follow up and compare with 
wolves which might also show comparable physiological as well as 
behavioral changes as a consequence of a change in social relation- 

Murphree et al. (1967, 1969) reported lower resting heart rates 
in a timid strain of pointers, while a more stable strain had a higher 

Behavior, Development, & Psychopathology of Cardiac Activity 205 

resting heart rate. These findings compare well with the test scores 
of high- and low-ranking cubs which are analogous to the timid 
and stable temperament types that Murphree et al. studied. These 
authors were only able to demonstrate bradycardia during petting 
in the stable strain, a phenomenon associated with the reactions of 
socialized dogs to familiar handlers (Lynch, 1970; Lynch and Gantt, 
1968). Bradycardia has also been reported in vertebrates in re- 
sponse to threat (Belkin, 1968). Again we have a paradoxical phe- 
nomenon; bradycardia evoked by both threat and petting but 
associated respectively with passive immobility or freezing and pas- 
sive submission, both behaviors possibly involving parasympathe- 
tic relaxation and cardiac deceleration. The bradycardia associated 
with threat or stress may reflect the animal's readiness to respond; 
a vigilance state which has been correlated with changes in elec- 
troencephalographic activity (Lacey and Lacey, 1970)- 

Gellhom (1968) has proposed that differences m temperament 
and behavioral reactions may be attributed to differences in sympa- 
thetic (trophotropic) and parasympathehc J?, 

tone. Schneirla's (1965) promising but as yet bt e es 

of biphasic sympathetic-parasympathebc processes jj 

togeny and organization of behavior is also re pvolain why 

erties. Thomas et al (1970). for example, ha temperament 

dons between the behavior of =>dotescen.s and the r ^ 
consteUations that were determined by a battery of S 

first few months of life. differences in nervous typolog)- 

The Pavlovian concept of ddferen^ 

(synonymous with ‘emperamen ) (^r dynamism), and 

Typologies differ in terms of bala, and^ excitation. Thus, a 

relative strengths noloEV or temperament ivould be 

strong balanced but dynamic tyP ^ , pss (neither overreactive 
characterized by adaptive respon balance between sympa- 

nor hyporeactive) where the horneo regulated (Kurtsm, 

thetic md parasympathetic systems is «eli gu 



1968). Such an animal would show appropriate behavioral reac- 
tions to tests requiring passive inhibition, approach, or with- 

The data on plasma cortisol secretion under stress and capacity 
to respond after ACTH treatment as well as the heart rate data 
accord well with the above concepts. It may be tentatively con- 
cluded at this level of analysis that dominant wolf cubs have a high 
sympathetic tone but do not overreact to stress (i.e., parasym- 
pathetic homeostatic regulation or balance is evident). Low- 
ranking cubs have a low sympathetic tone and show a hyporeactiv- 
ity to stress. Those of intermediate rank have a higher sympathetic 
tone but tend to overreact to stress. 

Follow-up studies over a 3-year period confirmed that these 
individual differences in temperament and rank order, established 
very early in life, were enduring provided the relationships with 
the Utter were not disrupted (as by the death of one key individual 
or the introduction of a stranger). 

These findings indicate that heart rate is a reUable index of 
temperament, but since both are determined geneticaUy and expe- 
rientiaUy, changes in social relationships may affect heart rate. This 
was not determined in canids, but the work of Candland et al, 
(1970) with squirrel monkeys shows that a change in rank is corre- 
lated -with a change in heart rate. They observed that 

Of special importance is the fact that when animals changed 
position on the (rank) order their heart rates changed accord- 
ingly, maintaining the curviUnear relationship. The impUcation 
of this result is that when dominance orders change, the heart 
rate of the animals changing position also changes. It suggests 
that rank determines the heart rate, rather than the reverse. 

This latter conclusion is unwarranted however without a de- 
velopmental study; their subjects were apparently unrelated and 
from diverse sources. 

Candland et at. (1970) found that there is an inverted U- or 
J-shaped curviUnear function with the lowest resting heart rates in 
middle-ranking animals, in contrast to the wolf where rank corre- 
lates more directly with heart rate. 

These authors ask, since they have also demonstrated a very 
similar correlation between rank and heart rate in chickens 

Behavior, Development, & Psychopathologi/ of Cardiac Activity 207 

Why would animals both high and low on the order show the 
higher heart rate? Or, conversely, why should midranking 
animals show the lowest heart rate? One possibility is that the 
noradrenalin/adrenalin ratio differs substantially in alpha and 
omega animals and has the result of generating different forms 
of behavior (flight or fight) while increasing the heart rate in 
both cases. 

Since neither of these species are predators, the observations 
of Funkenstein (1955) might account for the differences in cardiac 
activity between wolves, squirrel monkeys, and chickens, tie 
states that 

Experiments suggest that anger and fear may acHvate different 
areas in the hypothalamus, leading to production of nor- 
adrenalin in the first case and adrenalin in the secon . n 
more e^eriments are made, these possibilities mus remai 

Some of the most intriguing work in this field 
ported by von Euler. He compared adrenal secretions found in 
a number of different animals. The researc ™ adrenal 

supplied by a friend who flew to Afnca o Ruesch 

medullae of wild animals. Interpefing his 

ou. ,h., 7"^ “‘h K • rL 

atively high amount of nor-adrenali , flieht ad- 

the rabbiCwhich depend for survival Xals 

renalin predominated. also have a high 

that live very soaal hves (e.g., the 
ratio of adrenalin to nor-adrenalin. 

It may be, therefore, that exhibit 

noradrenalin (associated with aggressi j those with a 

tachycardia in socially o. assertive 

greater sympathetic . ^5^ ^^ith a lesser sympathetic 

and assume a higher rank should also be emphasized 

tone (and lower resting heart rat ^ ^ social reaction 

that passive inhibition rather than be correlated w«th 

to threat in low-ranking was evaluated in a 

a lower resting heart rate. This speculation 
subsequent study (see later). 


THE dog; its domestication and behavior 

Contrary to the notion that high vagotonia is an attribute of 
athletes and of dogs with superior physical stamina, what adaptive 
value would high sympathetic tone have for the wolf? The higher 
sympathetic tone experimentally induced in domesticated dogs 
(described in Experiment II) showed that such animals were emo- 
tionally more stable, more exploratory, and assertive. In the social 
context of the pack, such an individual would be more likely to 
survive under conditions of food shortage in a severe winter, and 
such wolves are usually the only ones to breed in a pack. How 
individual variance or heterogeneity is maintained in litters of off- 
spring to counter this unidirectional selection is an important ques- 
tion and deserves further study. 

As Linn (1974) emphasizes, "the relative effect of ACTH and 
plasma corticosteroids on the psyche of the animal may well be 
determined by the state of the ergotropic-trophotropic balance of 
the hypothalamus (GeUhom, 1968). Gellhom (op. cit.) has 
theorized that ergotropic-trophotropic balance is closely interre- 
lated with secretion of adrenal corticosteroids. Increased cortico- 
steroids reduce sympathetic hypothalamic reactivity, cause a con- 
current rise in parasympathetic hypothalamus reactivity and 
homeostatic balance is shifted to the trophotropic side." 

Field observations show that the lowest-ranking wolves are 
the least likely to survive a severe winter (again reflecting the find- 
ings in nonhandled rodents being less resistant to terminal starva- 
tion or cold exposure than those handled subjects that have an 
induced high sympathetic tone). The data on plasma cortisol levels 
and response to ACTH imply that such canids are essentially inca- 
pable of mobilizing an adapdve stress-response. This contrasts the 
overreaction to stress in nonhandled rodents; it may also account 
for the low resting heart rates in low-ranking carnivores, and such 
prey spedes of comparable sodal rank (as studied by Candland et 
al, 1970) may have abnormally high resting heart rates. 

Behavior, Development, & Psychopathology of Cardiac Activity 209 

Experiment IV. Heart Rate and 
Plasma Cortisol as Predictors 

of Temperament 

The following is an abstract of an extensive study by my colleague 
and student. Dr. J. Linn, representing an attempt to employ the 
testing procedures used in controlled laboratory conditions to a 
more uncontrollable kennel-rearing facility operated by army per 
sonnel. (For details of test procedures see Fox, 1968, 1971; Linn, 
1974; and Appendix III.) 

The plasma cortisol level and heart rate of one hundred and 
rune twelve week old German Shepherd Dog puppies was 
monitored prior to, during and after undergoing a 
cally stressful experience. The physiological parame e 
then examined for correlation with temperamen o g 

as they matured. 

Because of large standard deviations 
significant correlations between either of t e pa 
sumd and temperament. Plasma cortisol 
trend of prolonged elevation in * g j 

pies with the poorer temperament. (See igu 

There was a consistency in barline and fif- 

nations. The mean plasma ’^hape with the highest 

teen minute post-stress showed a P of the J. 

rated pups and the lowest rated pup highest cortisol 

Prior to testing the top rated puppies had ™ j 
levels and fifteen minutes after testing the lowest P 
pies had the highest cortisol leve s^ ^ 

The mean heart rate of the group P mean heart rate 

temperaments did not increase as mu stressful situation, 

of the passing group when Pf ’"'“ir^s was higher than 
Their mean heart rate^o mm P showed trends to 

in the passing group. Thus, P ,gi,o!ogical stress m fail- 
prolonged physiological P ^ standard deviation on 

ing puppies. However, the rang 


THE dog: its domestication and behavior 

I Standard Error of AAean 

(23 Baseline, Cortisol 
r~~l 5 ^Ainute, Cortisol 
M 15 Minute, Cortisol 


Figure 8. (From Linn, 1974.) 

cither side of the mean for passing/failing groups overlap too 
much to allow successful prediction of future temperament. 
(See Figure 9.) 

A critical reevaluation of this potentially very promising 
screening procedure for early puppy selection reveals one impor- 
tant methodological omission. Resting heart rates were never 

Behavior, Development, & Psychopathology of Cardiac Activity 


monitored biotelemetrically from jnjHal jueular vein 

Base heart rates were recorded f "Jn^'keMsee Fig- 

sample for plasma cortisol detenrunaho 
ure 9). 


THE dog: its domestication and behavior 

This prior stress served to segregate the pups on the basis of 
an inverted U function. The two groups of pups scoring best on 
temperament ratings (types 2 and 3) being intermediate between 
the reject pups (types o and i) which showed relative bradycardia or 
tachycardia poststress. The greatest increase in heart rate occurred 
in the highest-ranking pups when placed in confinement (Box) 
prior to release into the novel environment (Arena). All four 
groups of pups showed a similar increase in heart rate in the arena. 

The most significant finding is the heart rate recordings taken 
2 min after exposure to the novel environment (i.e., recovery). 
Return to a resting level was graded inversely in relation to the 
temperament rating, the lowest rating pups having the highest 
heart rates, reflecting a sustained tachycardia following stress. 

As in previous studies involving bradycardia in animals, insuf- 
ficient distinction of behavioral signs was made between the 
bradycardia of fear and of being petted or restrained by the han- 
dler. Both friendly and fearful dogs may show passivity (passive 
submission); monitoring of muscle tone (EMG) may help dif- 
ferentiate these two states of passivity in future studies. 

An additional factor which naturally reduced the variance be- 
tween categories of test subjects was in the initial selection proce- 
dure; extremely timid pups were discarded initially and were never 
used in the study. Had they been included, a more natural, 
heterogenous sample could have made a significant difference in 
the final analysis of the data. 

Experiment V. Bradycardia in 
Fear and Friendship 

Bradycardia was evoked consistently in unsocialized (feral) canids 
(see Figure 10). A 20-30% decrease in heart rate from "resting- 
alert" was usually recorded. The normal baseline of resting-alert 
was taken, since general locomotor activity causes a considerable 
increase in heart rate. 

Resting-alert heart rates were recorded biotelemetrically with 
the subjects alone in the testing cage and monitored via closed 

HEART RATE 250/mi n 

Behavior, Development, & Psychopathology of Cardiac Activity 213 

Figure 10. Heart rate decrease with contact in unsocialized coy 
X dog hybrids. 

„ aUn recorded when a handler 
circuit television. Heart rates were subiect, remaining 

entered the cage and sat 6 ft the handler sKxid 

passive and avoiding eye contact. ^ , physical contact (pel- 

up, slowly approached off and left the cage 

ting) for 1 min, and then slowly b 

repetitions for 3 consecutive <i3ys ^ ceneration coyofe > 

In the four unsodalized canids s subjects dunng 

dog hybrids), bradycardia devel<^ represent a conditioned 

repeated tests preceding Ficure n ) 

autonomic response or expectation. 


THE dog: its domestication and behavior 

SC02 Sitting 




* 5 sec * 

Figure ii. Precontact bradycardia. 

Tachycardia was frequently recorded when the handler ini- 
tially entered the cage and later when he stood up preparatory to 
approaching the animal. In the latter context, no subject attempted 
to escape although this cardiac response may reflect a readiness to 
escape — the flight response was blocked by the confines of the 
cage. In one subject, tachycardia was recorded as the handler 
withdrew atter making contact; this was correlated with attack 
intention movements (presumably evoked by the flight of the han- 

^ CD! Sitting 

Abroach Contact — 


Contact continuad 

Figure 12 . 

Behcmior, Development, & Psychopathology of Cardiac Activity 215 

Figure 13. 

dler). Over consecutive tests in the other ^^I'Z^p'fj^gbitu- 

approachgraduallydisappeared — aphysiolopca -ve contact 

adon (see Figures^ra and 13). When the handler made eye 
with the subject, a transient bradycardia was X 

(see Figure 14). 

I * 

' 70 fC 

Figure 14. 


THE dog: its domestication and behavior 


These cardiac responses corrclale well with Hediger's (1955) 
concept of flight and critical distance reactions in wild mammals 
(see Figure 15). Upon this proximily-related schema of behavioral 
and physiological reactions, those reactions of a sodalb.ed animal 
reacting to conspedes or to man. if it is tame or domesticated, may 
K- superimposetl. 

Behavior, Development, & Psydtopathology of Cardiac Activity 217 

Flight and critical distance reactions are then absent^ but phys- 
ical contact still evokes bradycardia. This was studied in several 
canids socialized to man, including domesticated dog, coyote, jack- 
al, and wolf. . , 

Petting reHably evokes bradycardia provided it is accompanied 
by an overt reaction of passive (friendly) submission. It is blocked 
by active (greeting) submission or general excitement (see igure 

16). . 

Petting bradycardia results in a 10-30% reduction m heart rate, 
similar decrease accompanied holding or picking up t e anima 
Figure 16). 


I Hold 

Chewi bone I 

Figure 16. 


THE bog; its domestication and behavior 

Alert Eating 

t Groin Contact tOff 

and muzzle seizure and piiming to the ground (see Figures 17 and 
18), both important areas of social contact in canids (Fox, igTid). 

Sustained bradycardia (but rates higher than during petting or 
handling) was recorded during exploratory and investigatory activ- 
ities (sniffing, looking at, or listening to novel stimuli) in all canids 
(see Figures 16, 17, and 18). 

This contrasts sharply with the transient bradycardia recorded 
in man during orientation and attention (Lacey and Lacey, 1970). In 
the vernacular, canids would be in a category of super- 
"sharpeners," a perceptual-cognitive style in man associated with 
great attention to details and to novel stimuli (or a change in the 
familiar) with low habituation rates. 

Heart rates during drinking were the same as or a little slower 
than resting-alert, while during eating, tachycardia (excitement?) 

Behavior, Development, & Psychopathology of Cardiac Activity 219 

Figure i8. 

J A-,. Pleasure response?) were frequently re- 
or slight bradycardia (p Lji„ eating, a sudden, transient 
corded. When '"“mi a freezing 

bradycardia , 3, n,ore sustained following an actual 

threat over the food ana was 

fight (see Figure ’ 9 ^- . obsen-ations, the sustained low heart 

From these compara ^ dominance (eliating passive 

rates during ,‘e( in an unsodalired animal (produong 

submission), aud ‘ gy „ common psychophysiologi- 

freezing or tonic im 


THE dog: its domestication and behavior 





10 sec 

Figure 19. 

cal response. Some of these behavioral reactions in which sus- 
tained bradycardia have been recorded are illustrated in Figure 20. 
The possible evolutionary significance of this phenomenon is dis- 
cussed subsequently. 


THE dog: its domestication and behavior 

General Discussion 

These observations and the literature reviewed present a somewhat 
paradoxical picture of the relationships between cardiac activity 
and various behavioral states. Paradox is to be anticipated when 
one is dealing with a complex neurohumoral homeostatic system 
such as the autonomic nervous system. As Gellhom (1968) ably 
demonstrates, paradoxical responses are often seen and can be 
explained on the basis of sympathetic-parasympathetic balance or 
ergotropic-trophotropic tuning in his terminology. Thus, an ap- 
parently paradoxical response such as bradycardia can occur in 
very different emotional states ranging from fear to pleasure. 

An important factor in predetermining the type of autonomic 
response may be the degree of sympathetic and parasympathetic 
tone characteristic of the individual or species in question. 

From the data presented, it may be hypothesized that wild 
canids (of high social rank) have a Wgh sympathetic tone and a 
high parasympathetic tone. Low-ranking, more fearful animals 
generally have a lower sympathetic tone coupled with either a 
weak parasympathetic tone or an excess of vagal inhibition either 
of which may lead to maladaptive stress responses. In Pavlovian 
terminology, the latter two typologies would be characterized re- 
spectively as weak and imbalanced nervous typologies and the 
former as strong and balanced. His fourth category, strong but 
unbalanced, would be seen in those middle-ranking canids that 
showed less adaptive mobility in inhibiting excessive sympathetic 
or parasympathetic reactions but were able to adapt better to stress 
conditions than the weak and unbalanced types (Kurtsin, 1968). 

The effects of early handling stress would seem to be creating a 
strong nervous typology with high sympathetic and parasym- 
pathetic tone. 

Domestication, from comparative studies of wild and tame 
canids (and other species dted), may have selectively reduced 
sympathetic lone rather than enhanced parasympathetic lone. It 
would be naturally advantageous to reduce the fright-fight-flight 
responses of animals in the process of domestication [and as dem- 
onstrated by Bcylaev and Trut (1975) the adrenal-hypothalamus 
axis responds in quantitatively different ways to stress in domesti- 
cated subjects). 

Behavior, Development, & Psychopathology of Cardiac Activity 223 

Great individual differences are evident in dogs of different 
breeds and temperaments, however. These differences do not con- 
tradict the above hypothesis on the effects of domestication but 
rather point to the original question of ergotropic-trophotropic bal- 
ance and dynamics or mobiUty in the Pavlovian sense. Such indi- 
vidual differences may stiU be manifest in the presence of reduced 
sympathetic tone or lowered ergotropic tuning. 

In his two classic papers on the effects of domestication and 
selection on the behavior of the Norway rat, Richter (1954) states 

Electrocardiographic records taken while the 
strained shoi^ in the case of wild rats, marked slowing of the 
heart — a definite bradycardia, and little or no c ange 
domesticated rats. ThL it appears that, as compared with wild 
ratS/ domesticated rats are much less vago onic. 

Is this conclusion ^fU°^night'response 

heart rates in wild and domesticated u -u-f of enforced 

(and associated tachycardia) is not mobi e canids) then 

restraint (analogous to passive inhibition m canids), 
bradycardia might be a highly adaphve response, 

Richter goes on to note that 

Domesticated and wild '“^ffpr'^exposure m cold, 

Woods, to the same form of stres ' jjj none 

fighting, or exhaustion ^om svnmnungjn the wil^ 

of these forms of stress had any adrenals, whereas in 

amount of ascorbic-add conten in , jevcl or 

the domesticated rat it he Sorbic-add 

else eliminated it altogether. In Hoses of ACTH. 

content could be depressed on y y better 

These results would thus indicate ‘ because of the more 

able to withstand various forms ot stress-^ 
active adrenals. 


THE dog: its domestication and behavior 

passive inhibition (tonic immobility) in order to avoid either attack 
by a predator or by a superior conspecific. Thus wild rats and wild 
canids show bradycardia under forced restraint, and both wild and 
socialized canids show bradycardia when being petted in associa- 
tion with passive submission and friendly greeting. The latter be- 
havior may have evolved, in the ethological sense (Chance, 1962), 
as a means of inhibiting or cutting off a potential attack by a social 
superior. This could account for the bradycardia occurring in two 
apparently unrelated contexts (see Figure 20). 

Increased parasympathetic activity (salivation, slowing of 
heart rate, and increased peristalsis and secretion of digestive 
juices) has long been recognized as a response in infant animals 
and human neonates alike to maternal attention (Spitz,i949). This 
parasympathetic (pleasure prindple) response in adult animals so- 
cialized to man is readily evoked by human contact and petting, as 
it is by one adult aiumal grooming a conspecific. 

Absence of such stimulation in infancy may lead to impaired 
growth (marasmus) and increased susceptibility to disease in both 
human infants (Spitz, 1949) and dogs (Bleicher, personal com- 

Thus, parasympathetic stimulation, an important aspect of 
maternal care and neonatal physiology, may be linked with so- 
cialization and potentiate the development of emotional attach- 
ments. This has been elaborated upon in detail by Schneirla (1965). 

In summary, therefore, contact with an animal socialized to 
man evokes relaxation and bradycardia — the classic psychophysio- 
logical response to petting or contact comfort. Contact with an 
unsocialized animal, however, evokes bradycardia associated in- 
stead with tension, freezing, or tonic immobility (see Figure 20). 
This latter cardiac response is probably an adaptive homeo- 
static mechanism to control for sympathetic hyperarousal. A 
comparable compensatory inhibition was recorded in a canid im- 
mediately after a fight with a conspecific (see Figure 19). Richter's 
(1954) conclusion that domestication reduces vagotonia therefore 
may be valid. High vagotonia would be an adaptive response to 
sympathetic overarousal which would occur in association with a 
wild animal's initial attempts to escape from restraint. Data on 
unsodalized canids support this view; marked tachycardia when 
approached but with escape blocked, bradycardia develops and is 

Behavior, Development, & Psychopathology of Cardiac Activity 225 

enhanced by physical contact (i.e., transition from freezing to pas- 
sive submission). With a lower sympathetic tone in a tame or 
domesticated animal, restraint or human contact would not 
mobilize a compensatory homeostatic vagal inhibition. 

But based on Richter's rather superficial data, vagotonia ap- 
pears to be more a function of context than of domestication per se, 
since human contact evokes bradycardia in a socialize 
enforced restraint evokes bradycardia in an unsoaa e appe 

wolf (M W. Fox personal observation). in 

Domestication has more likely influence e 
which vagotonic reactions occur and has lowere threshold 

and modified the adrenal-hypothalamic stress reac ° . ^ 

(a point demonstrated by Beylaev and Tmt 

docility over 14 generations). Consequent y, , "phasic" 

thetic tone relative to wild species, the ^^P . be 

vagal inhibition (rather than "tonic Richter's con- 

less in a domesticated animal. ® „ beti^een the adrenal- 

elusions helps clarify the interrelations P „ jystem and 

hypothalamic sy“'P^*®‘'^'P®” 2 ^rs%drome (Cannon, 1956) in 
would account for the sudden death ^ ^ ,g j animals which 

wild animals under restraint and in „ which may trigger an 

have an abnormaUy high ^^tta vaL^a^ark. .. 

excessive phasic vagotoma leading Pavlovian "collision 

This latter phenomenon, anatogous 10 
of excitation and Inhibition (but ea * § ^ account for the 

ganism rather than to a neurotic reac ' (be stress of 

apparent absence of a plasma co so 

restraint in low-ranking wolves. studies of temperament 

Kurtsin (1968) has ^viewed exten^ ^ 

or nervous typologies of ^trated clearly how different 

an conditioning procedures. He dem emotional or physical 

temperament types react to ^bilitv to stress and disease 

(e.g., total body ^“*“£,HalIv overreact, both auto- 

is greater in those breeds that o® adaptive behavaoral an 
nomically and behaviorally, an Future biomedical researc 
physiological inhibitory n the role of the autonomic 

might be advantageously ^‘’‘y^uwoarasympathetic intcrrelalion- 
nervous system and sympat ^ stress resistance in og 

ships in terms of disease susceptibility 


THE dog: its domestication and behavior 

of different breed and temperament. Again, as emphasized earlier, 
handling stress in early life might be instigated to improve the 
stress tolerance and disease resistance of susceptible breeds or in- 
dividuals. As Kurtsin (1968) emphasizes, sympathetic overarousal 
to stress, mobilizing high levels of adrenocortical steroids, may 
interfere with immune responses and impair normal healing by 
reducing the phagocytic activity of leukocytes. Hyporesponsive 
individuals are no less susceptible either. Autonomic and emo- 
tional (temperament) variables must be considered in understand- 
ing individual susceptibility or resistance to disease (see also 
Astrup, 1968). Given the wide variety of dog breeds, this could be 
a fruitful area for future research. 

Comparative studies of wild and domesticated cats 
(Leyhausen, 1973) and canids (Fox, 1971b) have shown that wild 
species are more active and responsive to novel stimuli, either 
visual, auditory, or olfactory. Domestication, therefore, may have 
affected the reticular arousal system and the response threshold of 
exteroceptors, a process which may have been mediated quite sim- 
ply by lowering sympathetic tone. Gellhom (1968) refers to this as 
ergotropic tuning and makes the following observation, which 
tends to support the above theory of the influence of domestication 
(artificial selection for temperament-emotional reactivity) on au- 
tonomic balance. A shift toward parasympathetic (trophotropic) 
predominance is proposed. 

Elimination of important afferent impulses tends to cause a 
shift in trophotropic-ergotropic balance to the trophotropic 
(parasympathetic) side. Thus, animals (cats) deprived of the 
organs of smell, vision and hearing show an increased reactiv- 
ity of the trophotropic system indicated by a lesser general ac- 
tivity and an increase in the duration of sleep. Such animals 
show also behavioral reversal. Nociceptive stimuli, which in 
the normal cat induce ergotropic effects, exert trophotropic ac- 
tions in cats which are blind, deaf and anosmic. 

The drastically reduced sensory input is analogous to the 
raised response threshold of exteroceptors proposed above. This 
view differs from that of Richter (1954) who may have misinter- 
preted the bradycardia of wild rodents as a general (tonic) indicator 

Behavior, Development, & Psychopathology of Cardiac Activity 227 

of vagotonia, whereas in fact it was an acute (phasic) trophotropic 
reaction to stress. Its absence in domesticated rats could simply be 
because they were essentially more docile and were protected from 
such stress by having a lowered sympathetic tone and a greater 
trophotropic tuning (or tonic rather than phasic vagotonia). 

Murphree et al (1967) have reported changes in heart rate in 
their two lines of stable and unstable (shy) pointers under different 
conditions. As in the findings with wolves and German s ® 

reported earlier in this book, the more outgoing sta e e a a 
higher resting heart rate (approximately 120/min versus 
the timid line). Contact with handler evoked a dear bradycarf a 
only in the stable line, the decrease in heart rate bemg shgh'ly 
greater when petted by a stranger. This latter resu ' 
by the authors, supports the hypothesis presen e 5„l,mis- 

petting bradycardia may be related to passive ( ^ J strange 
Sion, which in a sodalized dog, may be grea er 

'’"'Most interesting, however, was the 

nervous Une of pointers. There with an unfamil- 

rate when the animals were being petted— neimer 

iar nor a familiar person. . in order to monitor 

All subjects were restrained on a ,, , , .uis variable 

heart rates with a cardiotachometer. It is po ^ freely 

may invalidate any comparisons betvwen e yjowever, 

moving unsodalized canids , ‘Vupd m other contexts in 

judging from the abnormal behaviors de behavior of our 

the unstable line that they studied an ive are probably 

subjects when human beings were iio j„gs The subjects 

deaUng with two very nomal except for their 

used in the present study were beha ■ ^ jo man early in 

fear of man (because they had never een and lachycar- 

life). Consequently, human presence evo bradycardia, and 

dia, confinement triggered freezing* an jjj.jjciycardia — normal 
physical contact resulted m from a genclicallv 

physiological reactions. The unsla e P jp early life Their 

selected line had received much approached 

sustained low heart rates, absence o a rnntactcd, and catatonia 

and of any further bradycardia when contac 



suggest an excessive vagotonia or inadequate trophotropic balance. 
Further studies have disclosed an increased incidence of atrioven- 
tricular heart block, which together with low resting heart rates, 
would suggest that these animals have an abnormally high vagal 
tone (Newton et ah, 1970). This conclusion is further supported by 
the recent finding (Lucas et al., 1974) that these excessively fearful 
pointers lack the normal hippocampal theta rhythm (and had a 
tendency to sleep more than normal dogs). (This accords well with 
Gellhom's conclusions cited earlier.) The inability of these dogs to 
habituate normally to novel stimuli was correlated with an absence 
of normal hippocampal theta activity during wakefulness. It is 
normally depressed (desynchronized) in the initial phase of an 
orienting response but returns to theta rhythm as habituation takes 
place. These dogs also manifested catatonia (inhibition of motor 
function), which can be evoked in normal dogs by electrical stimu- 
lation of the hippocampus. 

A logical expectation would be that ergotropic rather than 
trophotropic enhancement would occur during such orientation/ 
attention processing. Novel stimuli, however, usually evoke 
bradycardia (as mentioned earlier in Fara and Catlett's study of the 
guinea pig). Lacey (1967) has described a similar attention 
bradycardia in man as a transient cardiac deceleration interpreted 
as a "preparatory" autonomic response preparatory to subsequent 

Graham and Ciifton (1966) have also reported transient 
bradycardia in man as a component of the orienting response to 
novel stimuli. Orbrist (1968) has shown that under these conditions 
cardiac deceleration is accompanied by a decrease in respiratory 
frequency and amplitude. These orienting- and attention-related 
bradycardias thus differ from the fear bradycardia, which is of 
much longer duration and is usually accompanied by polypnoea 
(Hofer, 1970). Thus, the entrainment or influence of respiration on 
heart rate is probably not significant. In petting bradycardia in so- 
cialized dogs, muscular relaxation and decreased respiration are 
associated with a decrease in heart rate. In a fearful unsocialized 
canid, respiration may be increased but bradycardia is elicited fol- 
lowing contact, and the animal is in a catatonic state of motor 
inhibition (see details later). 

Behavior, Development, & Psychopathology of Cardiac Activity 229 

Conclusi9ns: The Phylogeny 
of Submission — 
Bradycardia and Affection 

The following theory is an attempt to resolve the 

between the bradycardia of fear and friendliness, n ac , , 

be no paradox. The bradycardia associated wit passive 

submission may be a recent evolutionary deve opmen i 

social vertebrates from the bradycardia of fear, rharacteris- 

sive inhibition, freezing, catatonia, or tome ^ 

tic of more primitive vertebrates and inverte ra 

Consider the modes of reacHon imSy 

FUght or attack with effective antipred- 

(playing dead), in ’"^riy pr^-speaeS' is wgh^y^^^^ 

ator adaptation. In such a behavioral sta , associated with 

tained (as distinct from the transient bradycardias assoaat 

the orienting response and attention). nhvloeeny, and in 

It is often stated that ^nic im- 

the context of the present theory, this m y different species 

mobiUty is present in young mammals or r ^orc 

(deer, fox) and tends to disappear wi _„rcists throughout life, 
primitive vertebrates (rodents, reptiles), i P ^ gj by a sudden 
In the former species, it occasional y tnnic immobilit)’ in an 

stress, i.e., the shock of hysteria evolong tonic 

adult dog (see Figure zi) animal hypnosis (Vbl- 

This phenomenon has been bring about a rcsto- 

gyesi, 1966) and to sleeplike conflict situations where 

ration of homeostasis by de-arousa t actions preparatory to 

displacement behaviors resemble ce gjjgd that these steep- 

going to sleep [DeUus, ^967])- 1* ^ould b ^ by ek-c- 

like behaviors, associated with bradyca . 

trical stimulation of the carotid . ] displays, it 'S "'d ccc 

In the evoluHon (phylog«^"y> context may occur m 

ognized that some that are . por example, the e en 

other species in a very is thought to be the ei o u 

sive fear-grimace of primates and can.cts 


THE dog: its domestication and behavior 

Pjf ‘^'•sor of the submissive grin displayed in other spedes 
^ J’® signa CFox, 1971). A similar evolutionary emandpa- 

SecHo? of fear and contact- 

If the bradycardia causes a change in behavior foUowing some 

in ense noxious or fearful stimulus, i.e,, decreased activity and 

Behavior, Development, & Psychopathology of Cardiac Activity 231 

balandng of sympathetic overarousal, natural selection would 
favor inactivity if it was an effective antipredator strategy. 

Similarly, natural selection in social contexts, as where a 
superior (alpha wolf or dog's master) evokes passivity and submis- 
sive displays, could operate on these same primitive psychophysio- 
logical (cardiovascular-CNS) processes. Chance (1962), for example, 
has emphasized how passivity may cut off a possible attack y a 

social superior in primates. 

But this is not the end of these tentaHve correlahons. A passive 
or actively submissive (greeting) dog or wolf will usua y ® 
several infantile behaviors, such sodo-infanti e ac ons g 
characteristic of more sodal, gregarious mammals (Fox, 
regression to an infantile mode forces us to consi 
parental care in infancy. In socially dependent a u , . j 

a persistence into maturity of some aspects of e psy P j 
ical dependency of infancy (discussed earUer, w^er^ parentaj be_ 
haviors evoke parasympathetic arousal an ^ theory of 

arousal in accordance with Schneirla s [19 5] P 

behavioral organization). parasympathetic 

This initial dependency of the 1 of develop- 

stimulation (contact comfort) leads to a ^ persistence of 

ment toward sodal dependency j" of submission, greet- 

analogous physiological changes in essentiaUy inner- 

ing, and care-solicitng. In other w ' arousal and 

directed homeostatic function of para X P immobility) 

sympathetic de-arousal (as in the bra F jn higher verte- 

of primitive vertebrates becomes o er psychophysiological 

brates and instead occurs in sodal ofaffeclional 

dependency upon others forms the basts/ ^ sodal contingency 

bonds. Petting a tame snake or croco 1 reinforcement, 

without reward, whereas a a dog t^fUral dependcnc)’ is ver- 

The evolution of this psychop ys> ^jeprivalion of contact- 
ified by the wealth of data on pot thrive and ma> 

reinforcement in infant mammals. Z]in,vinc the loss of a mate 
even die. Bereavement and — ^ic of many species also 

or of a close companion in adult . ‘u^gjoiogical mechanism 
demonstrate how pervasive this P^^ ^ other-directed depen 

for social dependency is. Withou godal and leads a mon. 
dency, the adult organism is relatively asoo 


THE dog: its domestication and behavior 

or less solitary life. Deprivation in more sodable species (dog, 
rhesus monkey, and man) will impair the normal development of 
dependency relationships. Such overly inner-directed individuals 
have an extremely limited capacity to form normal social relation- 
ships in maturity (asocial, autistic, or even sociopathic symptoms 
may develop [Fox, 1974]). 

In conclusion, therefore, it is theorized that the parasympathe- 
tic nervous system (and cardiovascular CNS afferents) has evolved 
from an initially endogenous homeostatic mechanism to an 
exogenous, socially dependent mechanism is more gregarious and 
sociable mammals. This "social (evokable) homeostasis" or etho- 
stasis forms the basis for the development of affectional bonds be- 
tween animals and between animal and man.* 


Several studies of cardiac activity in wild and domesticated canids 
in various controlled conditions were described. Since changes in 
heart rate are indicative of sympathetic/parasympathetic activity, 
monitoring of cardiac activity provides a sensitive, quantifiable 
index of autonomic functioning and related emotional reactions 
and overt behavior. Developmental changes in heart rate were 
studied in several breeds of dog; with increasing age, between 2 
and 3 weeks, a gradual slowing in rate was found. Treatment with 
atropine demonstrated that this was due to the later development 
of vagal inhibition. 

Evidence was presented to support the hypothesis that heart 
rate, along with other measures of emotionality and behavior, are 

•In man, and possibly in other mammals, this socially linked and integrated 
psychophysiological mechanism may be the basis for empathy and altruism. (Lacey 
and Lacey, 1970, (or example, describe one experiment where immersion of the 
hand into cold water evokes bradycardia; a person observing another doing this will 
also show a transient bradycardia which is greater if he has recently immersed his 
own hand into cold water.) Parasympathetic control (corticovisceral feedback) is an 
essential component of meditation and certain Yogic practices; the physical and 
psychological benefits from such "mind-body control" for man are now being ob- 
jectively measured, so far with extremely promising results (Wallace, 1972)- 

Behavior, Development, & Psychopathology of Cardiac Activity 233 

valid indices of temperament. These factors, which as a multifacto- 
rial constellation make up what is generally termed temperament, 
were correlated with individual susceptibility or resistance to phys- 
ical and psychological stress and disease. 

To what degree such factors, and temperament per se, are 
inborn or innately predetermined, was partially answered by 
studying individual differences within litters. Environmenta in u 
ences, especially stress early in life, were shown to have ® ^ 

cant effect upon temperament, including heart rate and ot er e 
pendent measures such as plasma cortisol levels, dominance, an 
exploratory behavior. . t t • u 

Following the findings that those canids wit 
heart rates (either innately or as a consequence 0 . 

manipuIaKon) were superior animals in terms o ^ 

havior, learning ability, and resistance to stress, a g 
over 100 puppies was conducted. The heart rate was “ 
several indict of temperament evaluation fo«nd ^o^ 

valuable but not exclusive prognostic measure of later 
for training such dogs for miUtary work (guardmg and locating 

concealed mines). . chnwn to evoke a 

Using biotelemetry, contact and pethng reliably evoked 
clear bradycardia in dogs. This phenomenon to occur 

in dogs socialized to the handler. Bradycar unso- 

also following physical contact or wit reactions oc- 

cialized canids. The psychophysiolo^ mntexts was discussed 
curring paradoxically in such very 7ntexte 

in relation to parasympathetic-symp« u _ individual dif- 
These observations, together wit ,7 stress experience, 
ferences in cardiac activity and effects ° . Qn,ic tuning, elabo- 

were integrated with a relevant . differences in temper- 

rated by Gellhom, to account , ^an. The possibility 

ament, reactivity, and stress suscepb ■ jncreased parasympa- 
that domestication has contributed o differences m cardiac 

thetic (vagal) tone was explored; and su.sceptibibty to 

acHvity as an indicator of ^ for further study and 

stress were emphasized to be a vabd subject 
clinical evaluation. 


Domestication and 



In the foregoing material, some of the ""^„7fiffu- 

involved in domestication is discusred. O sp raisins pet 

ture research, in both farm animal husbandry 'n « pel 

animals, is the appUcabiUty of early ^ 

rearing methods are no less relevant m laboraton^ animal saence 

^“'T^frlarch studies reported herein add mjre^U^-r^unde. 

standing of the temporal “rgart^aHon o e , j^^rc re- 
itance in wild and domestic “"ids and their nyP^^^^ 
search is needed on the ®“l’l*e mtenn i 

vocalizations, although the study rep , ^ jog and the 

upthequesrionastotheon^n^M^ „,her 

possible effects of neoteiy an p^^^ 

behaviors. Domesticated dogs In subtle effects of domcsli- 

able statement for the reversibib^ Hosdc dofExperience -vith 
caHon and of the adaptability of ,he role of 

hand-raised wild canids adds j ju chapter 2 , and the 

sodo-ecological preadaptations . ,,icalion. This concluding 
genetic or species 

summary helps clarify and in eg • domestication and 

into a more concise appraisal oiin 
human relationships on canine 




Miscellaneous Aspects of 

It should be emphasized that movements and display postures are 
more stable under domestication than other characteristics (e.g., 
display structures); thus, there may be little interference with 
courtship, mating and other social behaviors. How an animal 
communicates and displays may be less affected by domestication 
than when and to whom it will display and when and with whom 
it will Interact. Interactions between different species may affect the 
amplitude and frequency of action patterns rather than alter the 
patterns of behavior per se, although in some instances, provided 
with the right contingencies of reinforcement, new behaviors 
within the animal’s repertoire but not normally manifest may 
emerge, e.g., canid mimicry of the human grin (Fox, 1971b) and the 
acquisition of American deaf-dumb sign language in chimpanzees. 

Evolutionary changes may be compressed and mimicked in 
domestication, genetic mutation, selection and migration, and iso- 
lation of populations under human influence occurring. Geo- 
graphic and experiential factors (e.g., sexual imprinting) may en- 
hance or reduce isolation in developing new hybrids and strains. 
Scott (1968a) succinctly states for the dog that 

The dog is . . . not in any large degree a conscious product of 
human ingenuity. Rather it has evolved under the influence of 
countless thousands of interactions with human masters. We 
can therefore think of the dog as a species which, on domesti- 
cation, entered a new habitat and underwent a process of 
adaptive radiation similar to that of a wild species entering a 
vacant ecological niche. It subsequently underwent further 
modification and diversification as it became divided into small 
local populations and selection pressure became relaxed in cer- 
tain directions and increased in others under the influence of 
the human social environment. 

The domestic environment can also induce a new phenotypic 
expression of the same (wild) genotype. Abnormal behavior and 
genetic instabilities may rise, as in the regression to a wild temper- 
ament, in overmagnification of a wild trait by a change in 

Domestication and Man-Dog Relationships 

threshold, or in disruption of temporal sequences such as sexual or 
maternal behavior. Examples include, respectively, shyness, fear 
of strangers, and neophobia which develops in some pups around 
10-12 weeks of age, as in the wolf cub normally; hyperaggressivity 
and proximity intolerance in certain breeds; aggressive dominance 
disrupting mating and prey-stalking and killing appeanng m 
bitches with pups. Repression of some natural behaviors may also 
occur, e.g., normal regurgitation of food for pups is often absent in 
purebred bitches and parental behavior incomplete or absent m 
male dogs, since the latter, kept for generaHons without contact 
with mother and pups, may show little interest in them and may 
even compete with and kill them. Many questions remain 
swered, notably why the apparent high mutagerac po en a o 
phenodeviant forms in the dog in contrast to t e “ some 

or is this mainly due to the dog having been rnginlv for 

4000 to 6000 years longer and the cat paving , P , 
one role (to catch vermin) and not selective y , ^ e j 
different roles as is the case in the various ^reed-c asses^of^dogs^ 
The question of the influence of coat co or o P influence 
an intriguing topic, since selechon ^^oa example, 

behavior and emotional rea'^^'^ity. Trumier 
notes that black Alsatians are livehe an g tempera- 

black is recessive, and some 

ment and carry the produce black offspring, 

black temperament are bred they P .. gj (hg possible 
Keeler (19^5) and Guthrie (^97^ ha- J, fox in 
significance of melanism in coIo p j-janee to social stress, 

relation to temperament, ioral and physical data from 

A multifactorial analysis of ^ graduate stu- 

over 60 captive wolves was con ly^ he found a coirela- 

dents, Randall Lockwood (1976). y^dult black color-phase 

tion between behavior and 'and more active and pas- 

wolves showed less temtonal ^nl^r-ohase wolves, 
sive submission than brown or an^^ ,vhen a wild and domestic 
Trumler refers to ' Hecks aw 1:0:50 distribution of re- 

species are crossed, there ^^iT^hn^dribut rather "qualities came to 
spective parent traits in the y ^ of the domestic animal, 

light which were those of difficult to interpret in the 

precisely what this statement implies 



absence of further data, qualification of the concept of prototype, 
and references to increased variance in Fj hybrids due to indepen- 
dent assortment of Mendelian units. This latter phenomenon is 
surely a key to increasing diversity and selection of phenodeviants 
in early domestication. Trumler may be confirming this and Hecks' 
law with what Konrad Lorenz (1970) demonstrated several years 
ago in his studies of different species of duck and their hybrids. He 
found that a hybrid of two species may show certain behaviors not 
present in either parent species but present in another, possibly 
more ancient or earlier evolved species. This is termed reactivation, 
a phenomenological construct which may be interpreted in terms 
of threshold and temporal sequencing of behavioral units, where 
omission, reorganization, or repetition of various units may occur as 
a consequence of either natural evolution (speciation) or domesti- 

Some of the specific and potential changes attributable to 
domestication in the dog are reviewed in this book. The changes 
fall into a number of more general categories relevant to the effects 
of domestication in other species as well. 

First, the changes may be genetic or environmental in origin, 
or they may be a consequence of more complex genotype- 
environment interactions (Fox, 1970b). Second, it is important to 
define the level of behavioral analysis from which conclusions and 
inferences are drawn; for example, certain consummatory acts 
(fbced action patterns) such as those associated with ingestive, ag- 
gressive, and sexual behavior may remain unchanged, while then- 
threshold, amplitude, and frequency may be increased or de- 
creased. Also the temporal organization or sequencing of action 
patterns may be modified (e.g., truncated at various junctions as in 
prey-catching and killing in canids) as well as the type of stimulus 
or release which evokes such behavior (e.g., a moving vehicle may 
become substitute prey for the dog or a person may release sexual 
responses in an imprinted bird). Generalizations, therefore, cannot 
be made as to the direction of changes in behavior (see Figure 1). 

Genetic influences are generally attributable to inbreeding, di- 
rected selection, and genetic drift. The removal of natural selection 
pressures and of such natural variables as seasonal changes in 
light, temperature, and availability of food can evoke rapid 
physiological changes (such as the multiple-estrus of wild felines in 
captivity, which in the natural state are monoestrous). Structural 

Domestication and Man-Dog Relationships 



changes, especially in display social marks) may ^ 

(horns, bumps, body ^tive breeding or more rapidly 

brought about slowly ‘trough sel^ ^ vanabics. 

by husbandry procedures sue 


THE dog; its domestication and behavior 

together with the social composition ot the captive animals (kept 
together in natural groups, free-ranging, or confined in groups of 
the same sex and age), can produce further changes in social be- 
havior, growth rate, sexual behavior, etc. Thus, the method of 
animal husbandry or mode of livestock management can greatly 
influence the animal's phenotype and presumably, over time and 
generations, the genotype as well. 

In an interesting experiment with rats, Hughes (1973)* 
evaluated three major environmental variables which may effect 
docility, namely, cross-fostering (of wild offspring onto a domesti- 
cated mother), rearing in an enriched environment (seminatural, 
complex cage as distinct from the small barren cage of standardized 
laboratory animal care), and early handling or gentling of the wild 
offspring. As might be anticipated, only the latter procedure had 
any significant effect in enhancing docility. 

Thus in order to evaluate the effects of domestication, the 
environment which the species is exposed to and is raised in must 
be known and operationally defined in terms of its actual and 
potential influences upon behavior, structure, and endocrine 
functions. Since the domestic environment is often unnatural to an 
extreme, abnormal yet adaptive changes in behavior, structure, 
and function may develop through phenotypic change or genotypic 
selection; atypical strains or genotypes may then emerge, quite 
different from the original wild form (see Figure 2, Chapter 9). 

Domestication may generally increase genetic variability and 
consequently lead to a greater degree of phenotypic plasticity, 
since the more unidirectional pressures of natural selection have 
been eliminated to varying degrees. Some researchers also believe 
that domestication causes a general degeneration, both physically 
and psychologically. This may be true of certain systems or struc- 
tures in some spedes, but as emphasized earlier, no single 
generalization as to the direction of the effect of domestication can 
be made. Degeneration, for example, may be extremely difficult to 
distinguish from infantilism or neoteny (paedomorphosis). 

A thorough analysis of domestication effects in any single 
spedes must not only take into account the genetic, environmen- 

•Hughes, C. W. (1973). Early Experimce in Domestiintion. Unpublished doctoral dis- 
scrtiition. University of Missouri, Columbia, Missouri. 

Domestication and Man-Dog Relationships 


tal, and experiential variables discussed earlier, it must also en- 
counter the limitations of comparative studies with a wild model 
ancestor. The latter, adapted to captivity for study purposes, may 
differ in many ways from one bom and raised in the wild, for 
which it is preadapted. Similarly, the domesticated species may 
differ from one that is raised under seminatural conditions or has 
actually become feral. The conscious or coincidental changes 
wrought by man's intervention must also be determined, for 
example, rigorous selection for docility may increase proximity tol- 
erance but may negatively influence fertility. Similarly, paradoidcal 
selection may lead to behavioral problems, as in selecting Alsatians 
to be highly sensitive, alert, and reactive; a number become 
hyperactive, overreactive, and extremely timid, also selecting an 
training a dog to be a protector or guard of person or 
set up a conflict with the demands to be soaable and fnendly a 
other times. Such coincidental or unidirected -changes and 
paradoxical sequelae to consciously directed selechon 
for specific utilitarian purposes must be iden e ® ^ 

complete understanding of the effects of domeshcation can be 


Origin of the Dog 

The origin of the domestic dog, *^P^esticated^e dog 

though!: is generaUy held that man ^riaUy^ 

because of its value as a hunting p association between 

(1965), cast doubt on this. His °f*“Xgo is a virtually 

Australian abongines and its main value is to 

untrainable canid, even when h g^^ement), to keep its 

keep the camp clean of garbage (an gggasionally to act as a 

human companions waim at rug r They are effective as 

watchdog, giving warning ° ™ forests, a fact supported 

cooperative hunters only m trop himtinc in a similar ram- 

by the use of the Basenji in Je early stages of 

forest environment. Presuma y 5 huntmg 

domestication may not have invo v Inter, 'vith solec* 

abilities except in suitable environments and > 


THE dog: its domestication and behavior 

hve breeding, did the dog come to fulfill a hunting role. Initially, it 
would seem that the dog was a camp companion, follower, and 
guard, and later its roles as hunter, draft animal, protector, and 
herder of livestock were developed. Domestication of the dog took 
place while man was still in the hunter-gatherer stage according to 
Dr. Barbara Lawrence’ who has found remains of dog in North 
America dated 8400 B.c., which indicates that the dog was the 
earliest of man's domestic animals. The dog later became firmly 
established in village farming communities, at which time, pre- 
sumably, selective breeding for particular utilitarian functions was 

Epstein (1971) has presented the most extensive and detailed 
review of the origins and descent of the pariah and other types of 
dog, with particular emphasis on those of Africa. He reaches the 
conclusion, based upon extensive critical review of archaeological 
reports, that the small southern asiatic wolf, C. lupus pallipes, is 
most probably the dog's ancestor, discounting jackal ancestry on 
the basis of chromosome number (jackal, 74; dog and wolf, 78). 
However, Chiarelli (1975) reports 78 chromosomes for the coyote, 
wolf, golden jackal. Cape hunting dog, and domestic dog; chromo- 
some numbers are therefore of questionable significance. 

Epstein (1971) concludes that 

Initially the domesticated dog was of no economic use to man, 
save for its doubtful role as a scavenger. Only gradually, and 
in the course of its diffusion, it became a utility animal — an ob- 
ject of sacrifice, of ceremonial or profane consumption, or em- 
ployed as a guardian of the home and flocks, in the hunt, for 
draught and for its wool, or merely tolerated as a scavenging 
pariah. It may be assumed that it was only after realisation of 
the usefulness of the first domesticated species that the idea and 
practise of domestication were transferred to other species. 

While this is a plausible hypothesis which I would support, it must 
surely refute his notion (and the widely held view) of wolf ances- 
try, since the latter would, because of its size and social behavior as 
a pack animal, be an unlikely carud candidate for Camp/settlement 
scavenger. Small contemporary subspecies of wolves in Southern 

•Museum of Comparative Zoology, Harvard University. 

Domestication and Man^Dog Relationships 


Europe and Asia have adopted a more jackal-like mode of a solitary 
scavenger because of shortage of available prey. It is improbable 
that early man lived in regions where prey was so scarce, but rather 
both the wolf pack and the human hunting-gathering group 
shared a comparable niche rich in available game. The role of 
scavenger would then be assumed by jackal- and dingo-like canids 
in association with human campsites and following wolf-pack 


With the advent of agricultural settlements and increa^ng de- 
struction of natural habitat, some wolves may have become 
scavengers close to such settlements, while others move r ^ 
away into more remote uninhabited regions. The ormer wou 
have been a threat to the Uvestock that were J 

date and would have certainly been discourage . Jac a s, / 

are smaUer in size and less powerful than wolves 
been tolerated more since they would be bttle Yem^f “ 

people. In a parasitic/symbiotic mode compare e 0 domes- 

jackals and feral pariah dogs, the primihve pro otyp j^ggegted 
ticated dog was undoubtedly tolerated by early man as 
by Epstein (197X)]- and this prototype ^^/dcateS 

wolf-like. Therefore, the ’ (possibly dingo-Uke) 

dog arose from a more primitive pro ^ man's interven- 

which evolved from the wolf/jackal P 
tion and prior to its initial ^(1068) noHon of the affin- 

One must seriously queshon Sc ( 9 and pack 

ity between dog arid wolf m " evidence to support the 

formation (which, argues, is s g First, 

view that the wolf is the ancestor o -vailability, distribution, 
environmental influences, especia y fnrmation (Fox, 1975a)- 
and type of prey affect sociability an^pa^^^^^ adopt^a 

For example, in Italy, wolves tend ^ coyote. The 

scavenging mode of ^^stence simto n,ay be 

latter two species, normally living plentiful- Thus, envi- 

found in packs and in areas where ^ there is a compara- 

ronment influences sociability, an yj,i5 influence, keep- 

ble picture complicated by man s m territoriality and has a 
ing a dog on one's py°P^' free-roaming and ho/oeless 

socifugal or dispersing effect, dominance hierarchy a 

dogs in the same locale may establish 


the dog: its domestication and behavior 

hunt in a pack, provided food is plentiful. This was observed on a 
recent field trip to Southwest India where a study of village pariah or 
pie-dogs revealed this environmental influence on social behavior. 

Studies of Pariah Dogs 

Observations of home-owned free-roaming and feral pariah dogs 
in India revealed the complexity of their social organization in the 
typical rural village environment. Adopting and socializing one 
adult female and following her interactions with neighboring dogs 
added further insights in support of the following tentative 

There are basically three types of pariah dog: (i) home-owned 
and not inclined to roam more than a few hundred yards from 
home, (2) home-owned but free-roaming, (3) ownerless and free- 
roaming, with or without its own home-base territory, a den, or 
shelter. Gregariousness increases from (i)-(3), attachment to man 
having an intraspecific socifugal effect. In (1) the dog often man- 
ifests relative dominance (Leyhausen, 1973) in that within its 
home-base territory it is dominant over intruders. In (1) its 
foragingihunting range may be restricted by two factors, namely, if 
it is given food by its owner (which is rare) and if it is subordinate 
to neighboring dogs. Foraging and hunting ranges overlap, and 
consequently, where dogs meet away from their home bases, abso- 
lute dominance is seen. While a dog may drive a neighbor off its 
(owner's) property, it may be subordinate to the same dog on the 
neutral territory of a shared foraging/hunting range. Thus, attach- 
ment to man and place has a socifugal effect, while sharing of the 
same food area leads to the more typical dominance-subordinate 
hierarchy. Here, competition over available food concentrated in a 
limited area increases conflict, and an absolute dominance hierar- 
chy is established. Interestingly, though, this constitutes a loose 
social unit (not a pack per se) and pariah dogs of types (1) and (2) 
especially will temporarily pack together to hunt deer (an activity 
encouraged by villagers) and to drive off a strange dog that enters 
their shared range or collective territory. 

Domestication and Man-Dog Relationships 


Different relationships between the sexes, between dogs of 
different ages, and females in heat and with pups also influence 
the type of interaction between conspecifics of all three classes, 
ranging from active and passive submission to indifference or overt 


Type (3) dogs may aggregate more frequently and form tem- 
porary packs, sleeping, foraging, and hunting together, since they 
lack the sodfugal influence. of having an owner and home-base 
territory to defend. In larger villages, where several sources o 00 
may be present (butcher and baker stalls), dogs may set up a tern 
tory around a source and keep others away. Many sue fS® •'re 
homeless and belong to type (3), but competition f 

food source sets up a territorial situation ana ogous o , 

based dogs of type (i) and (2). In one village, t 

pariah dog that was the most dominant dog m e < 

having unchallenged freedom of movement an ^^ . .. 

sources. In summary, the influence of j_(r£, 

more dogs with a home (shelter with or wi ou 

sodfugal territoriaUty which is compUcated 

dog. Lr compel. .1 copemle 

defending their shared range or collec p,npe docs of all 

dent free-roaming and feral dogs. With sh-^d ^ S - ^^^8 
three types may be involved. by these socifugal 

upon a social dominance hierarchy, neiehborinc dogs can 

factors, but even so, this loose soaal "^‘Shbo^g g 

form a temporary pack in a collective 

range/territory against 5 bsequently, though, the pack 

forest or jungle close to the village S^qu >; ^ f.u-, 

dissolves into a loosely structured „»urn to. Also, ihe suppH 

that some dogs have home terriloncs o deters pack fornu- 

and distribution of their usual email numbers m order ti» 

tion, since they must forage , optimi/o the utili/atum oJ 

minimize competition and confl 
such resources (see Figure z)- 


THE dog: its domestication and behavior 

Figure 2. Indian village pariah dogs showing a typically emaciated 
bitch nursing pups and males forming a temporary pack around a 
female in heat. Village dogs tend to establish territorial zones 
around local food sources but in the absence of such may form 
mixed nomadic packs. 

alone. In the latter, where dogs share the same home range with 
others, there is some form of sodal organization as a loose unit, 
since they will band together and drive off strange dogs, as I also 
observed in India. Presumably the interrelationships among 
domesticated dogs with homes, homeless village-resident scaven- 
gers, and more peripheral feral dogs are a complex interplay of 
territoriality, competition/cooperation over food (garbage and wild 
prey), with each other (and with wild species such as jackals), and 
social dominance-subordinate relationships relative also to the 
proximity of home base or natural den/shelter (i.e., the center of 
each animal's territory). CTerritorial zones may overlap and several 
dogs may share the same hunting/scavenging range). Sociability 
will vary, therefore, not only in terms of the individual's tempera- 
ment but also in relation to these sodo-ecological variables of space 

Domestication and Man-Dog Relationships 


(place) and availability and distribution of food. Since pariah dogs 
may live singly or in packs, the flexibility in their social behavior 
points more to environmental adaptations than to support of the 
view of wolf ancestry as proposed by Scott (1968a). Menzel and 
Menzel (1948) conclude that 

The question of the pariah dog is among the most interesting 
of zoological problems, particularly from the point of view o 
racial history. We can be quite sure that an examinahon of the 
history of the domestic dog in all its aspects would reveal that 
there is scarcely a single facet that might not be il uminate y 
research into the problem of the pariah dog. . . . 

In spite of varying theories on the descent of the dog, mMt au 

thors recognize h^o distinct sub-groups of the genus m the old 

world which differ from each other in raaa is ““T 

Northern and the Southern Dogs. The 'nike 

s..*™ s,o«p. S>»d„ do., 

those in the Northern group) back to tne 

kind of Canides. He writes as follows: ro than 

Flood there existed a type o( Canides 

the wolf, distributed in the same area “ 

number in the OTUsequent y ^pre^ 

Australian continent. This kind is d dinco." 

rieties ... in the South it is represented by the dingo 

.ueinc nf the domesticated 

The pariah dog is a prototype Pf P ^naIoEOUS to those of 
dog, Uving today in India ‘ communities. It shows a 

early agricultural man in small vi g formation— which 

high degree of social flexibility so ‘ conciusions pro 

in no way supports or negates a wo ciudvinc the pariah dog. 
or con can be drawn of wolf ancestiy fmm stuuj g ^ 
but rather, they manifest a degree o s unique to dog or ivolf 

tive to the environment and which _.,nd jackal may form 

Under certain conditions (Fox, ^ 9751 ’ may break up an 

packs from a loose social unit, an w more solilaiy coyote 

follow an adapHve social model typical of the m 

and jackal. , , ,,rban and rural dogs in llw 

Studies of free-roaming “bundance of food (prey m 

United States similarly show tha " . V urban areas when- fo" 
rural areas) dogs svill form packs, " 


THE dog: its domestication and behavior 

is less plentiful, packs are rare and a solitary mode of foraging 
usually disrupts pack formation with a few exceptions. Dogs with 
homes (and usually, therefore, a constant source of food) do not 
generally roam far; they tend to be territorial rather than running in 
neighborhood packs and the latter, when seen, are usually merely 
temporary groups of males around a female in estrus as detailed in 
Chapter 3. Thus, the contention that since dogs are highly social 
like the pack-forming wolf, the wolf must be the ancestor of the 
dog, is untenable. 

Three other factors supporting wolf ancestry must also be 
questioned. Scott (1968a) states that dog and wolf have very similar 
behavior patterns and vocalizations. The latter is certainly not true; 
the range and variety of howls recorded from a single wolf con- 
trasts the limited range of howls in domesticated. dogs, as well as 
other vocal characteristics discussed earlier. 

Behavior patterns are very similar in dog and wolf, there being 
a closer affinity between these two species than between dog and 
coyote or jackal and other canids reclassified in terms of behavioral 
rather than structural similarities (see Figure 1, Chapter 2). While 
this evidence may lead to the conclusion that the dog is a domesti- 
cated wolf, it equally implies that they may share a common ances- 
try prior to domestication and that the dog was a dog before it was 
domesticated. This idew is supported by the fact that behavior 
patterns per se are influenced little by domestication; how an ani- 
mal behaves is more or less phylogenetically fixed, but when and 
to whom it behaves as well as the threshold and sequencing of 
behavioral units is affected by domestication and early experience. 
Structure is more influenced by domestication than behavior; a 
bulldog, Irish wolfhound. Chihuahua, and dachshund, structur- 
ally very different, share the same basic behavioral repertoire. 

The change in structure which most archaeologists and 
taxonomists recognize as a consequence of domestication is the 
reduction in tooth size; even a large breed like the Irish wolfhound 
has small teeth relative to its skull size and in comparison to the 
wolf. This may, however, simply indicate that this breed type is a 
giant mutant from a medium t5rpe having a tooth size more com- 
parable to a large jackal or small wolf. So a small wolf has been 
sought as the probable ancestor of the dog, and the Asiatic wolf, 
Canis lupus pallipes, is now accepted by most taxonomists and canid 

Domestication and Man-Dog Relationships 


ethologists as the dog's ancestor. Yet there is no evidence of a 
transitional form; all that excavations have revealed in the Middle 
East to date are remains of a small wolf, large and small spedes of 
jackal, and what is thought to be dog, with skull and jaw fragments 
which overlap in measurements with the former two spedes and 
so make identification difficult (Clutton-Brock, 1969). The contem- 
porary native pariah dog is very similar structurally to these 8,000- 
to io,ooo-year-old canid remains. Berry (1969)/ important 
paper relative to this archaeological dilemma, points out that 
natural environmental changes can mimic changes attributed to 
domestication, e.g., a reduction in tooth and jaw size may be ims 
identified in the case of the wolf as being due to domesticahon. 
Pre-Pleistocene wolves were of much larger build in t e e 

East than the existing subspecies today. 

There is a cline of blotched tabby in European 
to the coat pattern thought to be an exclusive trait 
Berry concludes that 

wild cats similar 
of domestic cats. 

even for a single species, it may be extremely 
down criteria to distinguish between domesdca 
domesticated forms . . . there is no reason to beue 
domestication per se will alter the phenotype or 

part of the genotype. . , 

° j r r f has been jdcn* 

Further review of the earliest remains o p c. as the 

dfled as C. familiaris gives dates of (i975) 

earliest date of domestication. Interesting y. jineo by 20,000 
ports that the Australian aborigines prece e dated around 

y®3rs, since the first signs of dingo ,„d dog alike re- 

10,000-8,000 B.C. Origin of dingo and domestic 
main an enigma archaeologically. v,nlds that when it was 

General (but unfounded) consensus denied 

first domesticated about 10,000 ,,, hwus patUV^) 

mm a wolf, possibly the Asiatic wo ( jj-po-like canid "as 
*aeological records, however, show that a (Macinuwh. 

'Widespread throughout Europe in the S b pn- 

iq7ciu:__ ? .. .u-. dnmeshc dog ' . 

"mespread throughout Europe m o- - 5 denveo t 

■975). It is my conTention that the df ddfen; 

anly from this prototype ^'’”’1^ j -vith mdigcdcds 

place.; ..„c crossbred w'f ‘ m.ile.-nu 

P sees and times this canid was guch 

° produce some of the more wolfish bre 


THE dog: its domestication and behavior 

and the husky. Although the dingo in Australia is somewhat like 
the coyote in its social behavior, being relatively solitary, living in 
pairs, and not forming packs, it is the ecology that has determined 
this kind of social behavior. If prey were more abundant, pack 
formation might be possible. Today, the domestic dog is capable of 
reverting to the wild (becoming feral) and surviving well, either 
singly, as a scavenger or opportunistic hunter, or combining with 
other dogs and forming a pack. The pack instinct of the domestic 
dog and its responsiveness toward a pack leader may well be the 
basis for its integration into the human family. In other words, a 
transference of the pack relationship to a family allegiance occurs, 
and this natural instinct greatly facilitates domestication and train- 
ing. In fact, if socialization is delayed, the dog is virtually untraina- 

Behavioral Effects of 

Further behavioral evidence of wolf ancestry from Scott (1973) must 
also be chaUenged . He suggests tt\at the muizle-bite greeting ritual 
of the wolf (detailed by Fox, 1971b as a spcdes-typical action) was 
wlcctively eliminated in domesticating the dog since it is frighten- 
ing to man. Having kept wolves myself and knowing others who 
h.ive raised them and who arc familiar with their behavior, there is 
no anxiety around such interaction. Also some northern dog 
bmeds which probably do have recent rvolf origin (malemute and 
husky) show this muzzle-biting behavior and breeders have no 
concern or anxiety about this trail. 

Domestication and Man-Dog Relationships 


surely recognize a socialized canid independent of its tail! This 
attractive conclusion is unwarranted however. It is not so much the 
structure and carriage of the tail that is signihcant (even though the 
Spitz-type dogs always carry it high) but the differences in tail 
displays in dog and wolf. If it is accepted that structure (cur y or 
docked tail) changes more under the influence of domes ca on 
than behavior (tail postures in communication), then t e wo an 
cestry of the dog seems even more remote. For examp ^ 
threat posture of the wolf, the tail is held verhca y 
angle of 75°-85° from the horizontal (of the back), w ® ^ 

it is curved as an arch over the back, even f j 

eastern pariah dogs) that carry the tail low in e sa p 
the wolf when at rest (see Figure 3). mat ourports 

Having negated aU “TndSsty ^ 

wolf ancestry to the domesticated the dog 

supporting archaeological f ^J^ted his/her specu- 

remalns unsolved. Lorenz (1975)- who ^ j},^ 

lationof a dual wolf-jackal dog ancestry, ^ as with the case 

general consensus in favor of wolf ance^, g f^^enzel (1948)/ 
for the jackal, with no clear evidence. detail, point out 

who studied contemporary pariah dogs 1 _ ^ ^e 

the dilemma that one cannot today 1 independent of 

domestic since the latter may become e . ] coyote, but 
man. Dogs may also hybridize wit wo ' ^d usually 

presumably ethological and ecoli^ca a q 

prevent this. The point is that , panics which, like a wild 

familiaris in the wild today other than e _ p£ phenotypic 

of phenotypic uni- 

species, will eventually breed to a g 

formity after a few generations. j pif jj the supra 

Aiiother dear cUstinction between dog en 

caudal tail gland (Fox, igp^)- f ,he taU, is active m the 

stripe of dark hair on the upper surfare ^t^^ , Furthermore, if 

wolf, no odor can usually be detec e ^ jp me domestic 0^ 

there is a distinctive hair mark over jjy triangular as 

the mark (of darker or thicker m (he wolf- This is s 

coyote and jackal and not a thin stnpe 

human nose, distinctively ■ Hogs' 

’When an odor can be detected, it is, 
contrast to the sweet-mown hay odor o 

Figure 3. Dislinclivc trails of wotf and dingo, (a) Vertical tail in 
dominant uvif (in center); (W arched tail in dominant dingos—all 
asserting high rank; (c) and (d) rank conflict between dingos on in- 
Iroduclion, including aggressive clasping and (inhibited) cheek- 
oriented Hte; (e) in same period together wolves form an integrated 
pack in contrast to more individualistic dingos: (P dominance- 
submission in F. coyote X dogs; note doglike arched tail position. 

Domestication and Man-Dog Relationships 


strong evidence against recent wolf ancestry in the dog. (See Table 
I for a general overview of wolf/dog differences.) 

Comparative studies on the behavior and development of wild 
canids has enabled us to identify a number of changes, whic in 
the domestic dog may be attributed to the effects of domes ca on. 
For example, the wolf reaches sexual maturity at 2 years ot age, 
while other wild canids attain full sexual matunty at i year of age 
In the wolf, this delayed sexual maturaHon might have important 
social consequences, in that the young will stay amn" ° sexual 
year to help adults raise another litter. In Domestica- 

maturity is reached at a much earlier age (6-9 mo • , ^ 

tion, therefore, has accelerated the opment of ^ndocnne 

glands associated with reproduction. Rela e ° 
full sexual activity in the wild canids is the nmerg . , in 

dominance relationships, and defense ° time base at 

the domestic dog, these behaviors appe central emo- 

12-18 months of age. This suggests Uj ^jp^i 

tional aspects related to full sexual ma u ty ,j^c>ueh domestica- 
the endocrine aspects of reproductive behawor ,,,„al 

tion. For example, by 1 year of age a eoy against in- 
maturity and at the same male rivalry fights. In 

truders and wiU engage in dominan attained much ear- 

the domestic dog full reproductive po aeuression toward in- 

lier in life, while problems assoaa e develop until 

truders and dominance fights wit t e n sperm seasonally, 

a later age. The males of wUd “™.^/P™ ,ntly fertile. Whereas a 
while in the domestic dog the male 1 ^ the dog 

wolf may show specific mate Pf® ^ 'jij make selective bree - 
may have been eliminated, since jj ( sk if the stud or bite 

ing under the choice of the owiier a ^ff « 
refused to mate with a selected an beagles, and o 

Comparative studies of identical conditions, 

domesticated breeds, all raise {jg dogs show nme 

shown that on separation the o observations 

distress. It can be*^ concluded ^^pendent than the ».ld 

domestic dog is basically mu the easier it is to train 

species. Theireater thedependen^>- ex.rcm 

animal. Hand-raised wolves and 7 potonousl) 

able and friendly toward the another consequence 

train. It may be proposed, there 

Tnble I. 


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.iggressivc hip-slam common rare except in wolflike breeds 

vertical tail in threat* usual display in dominant wolf absent — tail arched in threat 

T.iblc I. (nmliiiunl) 

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•Wolf-<log differences may imply separate ancestry rather than effects of domestica- 
tion per sc. 

Domestication and Man-Dog Relationships 


domestication has been to make the domestic dog extremely de- 
pendent. The degree of dependency varies from breed to breed. 
For example, malemutes and huskies are aloof and are much more 
difficult to train than the more dependent and willing terriers and 
toy breeds. In the toy breeds, there is not only a greMer 
dency but also a neotenization or infantilism, whereby t e P 
structure of the adult animal more resembles an infant, le m 
with the relative immaturity of the structure is the p^e ua ° 
infantile behaviors into adulthood. How much 0 t is 
and how much is related to the way in which t ^ . 

animal is open to question. The capacity to re am 
haviors into maturity must be genetic.* Cornpara infantile 

the wild canids reveal that the wolf has const era ^ 

behaviors (which are called derived infanti e ac 0 
compared to other wild species. integration and 

dency to foUow supenor animals, help njiveness to a 

coordination of pack activity, . j ,i,e domestic dog. 

leader or parent figure is no less evi Jemonstrable dcpen- 
However, because of the greater de^ possibility for de- 

dency in the many breeds of domestic S' time, it 

veloping emotion^ disorders is ewance , . ^jy dependent 

isamorefulfiUingpetforthosewhoneedanextrem y 


Relationships and 
Human Needs^ 

voung people 

Human relationships are now „ children for a 

having any children or are delaying citizens, retired 
of years after their marriage, en 

are not 

Domestication and Man-Dog Relationships 


parent, then it should not be a surprise that both dog and child 
under certain conditions may develop analogous or homologous 
behavior disorders. These can range (Fox, 1968, Brunner, 1968) from 
psychogenic epilepsy to asthma-like conditions, compulsive eating, 
sympathy lameness, hypermotility of the intestines with hemorrha- 
gic gastroenteritis, possibly ulcerative colitis, not to mention sibling 
rivalry, extreme jealousy, aggression, depression, and refusal to 
eat food (anorexia nervosa). 

Types of Relationships 

The following is an arbitrary classificaHon of various types of rela- 
tioLCs which may be established between the owner and the 
dog (fL, 1976c): object-oriented; 


guide for a bUnd person, or is used foxhound The use 

driving cattle, or for sport, such ^ increase today. People 
of the dog as a guard is paranoid about crime and vio- 

Uving in suburbia are opberman pinscher or German 

lence and will buy a dog such More recently dogs 

shepherd that they will have clinical psychologists 

have been used as camne the patient (Corson ft 

utilizing the dog as a therapeutic bndge witn t F 

»l-, 1975)- 

Some Consequences of 
Pet-Owner Relationships 

It is the 
can be the 

h^ncnnn doc and owner that 
close s^biotic Emotional and psychosom.v 

he foundation fora numoeroi 


THE dog; its domestication and behavior 

widows, and widowers whose offspring might now be living many 
miles away have a need for a close companion, be it cat, dog, fish, 
or parakeet. It is not only the patterns of human social life that have 
changed over the past 20 or 30 years, but also human needs as well. 
The need for companionship, for example, is exaggerated when 
families are separated and when people are lonely and alienated in 
a depersonalizing urban environment. The more dependent the 
pet is for some owners, the more fulfilling it is as a companion or as 
a child substitute. It is this dependency, however, that opens the 
doors to a number of psychosomatic and psychogenic emotional 
disorders, some of which are analogous to those described by child 
psychiatrists. I believe, therefore, that the incidence of some of 
these disorders will increase and that the veterinarian in small 
animal practice will have to be on the lookout for such disorders in 
the near future, if not today. 

Critics might say that to attribute a dog with humanlike emo- 
tions and needs is to be unscientific and anthropomorphic. Re- 
search has shown, however, that the developing brain of the dog, 
its unfolding pattern of socialization and other critical and sensitive 
periods during development are very similar, and sometimes iden- 
tical, to the same phenomena recognized in the human infant, 
although they develop on a different time base (Fox, 1971a). The dog 
has basically the same limbic or emotional structures capable of 
generating specific feelings or affects reflected in overt emotional 
reactions and also in changes in sympathetic and parasympathetic 
activity which are linked with psychosomatic and emotional disor- 
ders. Add to this common neural substrate shared by dog and- 
human infant the important variable of attachment which is a con- 
sequence of socialization, as between dog and owner and child and 

Domestication and Man-Dog Relationships 


parent, then it should not be a surprise that both dog and child 
under certain conditions may develop analogous or homologous 
behavior disorders. These can range (Fox, 1968, Brunner, 1968) from 
psychogenic epilepsy to asthma-like conditions, compulsive eating, 
sympathy lameness, hypermotiUty of the intesHnes with hemorrha- 
gic gastroenteritis, possibly ulcerative colitis, not to mention sibling 
rivalry, extreme jealousy, aggression, depression, and refusal to 
eat food (anorexia nervosa). 

Types of Relationships 

The foUowing is an arbitrary classificaHon of ° ' 

tionships which may be esfabUshed ° 

dog (Fox, 1976c): The most 

dependence; transp«sonal re^ d ^ ,^^.^_^^P 

general one is simply neea aepenuti ^ j 

Irai. .h. «,d.l in ''“rr.t 3 ronr.(rSS.n 

Another relationship with ^ dog P^J^ j ^ guard, as a 

working relationship where the og i P ^ herding sheep, 
guide forabUnd person, orisused orwork^^^^^^^^^^ 
driving cattle, or for sport, such increase today. People 

of the dog as a guard is paranoid about crime and vio- 

Uving in suburbia are ^ Doberman pinscher or German 

lence and wiU buy a dog sue . More recently dogs 

shepherd that they will ‘ ‘ 15,5 by clinical psychologists 

have been used as canine co- P patient (Corson el 

utilizing the dog as a therapeutic bndge with P 

at., 1975). 

Some Consequences of 
Pet-Owner Relationships 

It is the close symbiotic .md psydi>«.'ma- 

can be the foundation fora num 


THE dog: its domestication and behavior 

tic disorders. For example, the dog that is overindulged and is 
raised literally as a child substitute may develop a variety of be- 
havioral abnormalities when its relationship with the owner is 
threatened — as by the birth of a child, by the introduction of 
another pet, cat, or dog into the household, or by the arrival of 
house guests. Separation from the owner due to the owner being 
sick or the dog being boarded when the owner goes on vacation 
can similarly trigger behavioral pathologies. These include unpre- 
dictable aggression, depression, anorexia nervosa, hivelike reac- 
tions and pruritis, excessive eating, sympathy lameness, convul- 
sions, asthma-like conditions, cardiospasms, vomiting, and intes- 
tinal disorders, including hemorrhagic enteritis. The overindulged 
dog may also be underdisdplined and when it reaches full sexual 
maturity it will behave like a socially maladjusted "canine delin- 
quent." It may effectively win the dominance fight with its owner, 
and it may become the overlord of the household. Such socially 
maladjusted dogs are extremely difficult to handle on their own 
territory and can be no less difficult to handle in the hospital. It is 
important for the veterinary surgeon to establish his dominance 
over such a dog, and it might be discretely done in the absence of 
the owner. 

In making a diagnosis, it is important to look into the family 
background of the pet, and to be aware of the dynamics in the 
household and to be alert to any recent changes within the home 
environment. Some emotional disorders may disappear spontane- 
ously when the animal is hospitalized and is removed from such 
aggravating circumstances. A careful differential diagnosis must of 
course be made and the possibility of allergic, organic, and other 
infectious causes must be considered. The real crux of the problem 
is that the close symbiotic relationship can be the genesis of a 
number of dependency disorders in the dog which can be ex- 
pressed behavioraliy or psychologically and somatically. 

Domestication and Man-Dog Relationships 


been neotenized nor have they been made much more dependent 
than their rvild counterpart. The kind of person who will prefer a cat 
to a dog as a pet is perhaps less Ukely to need to indulge such an ani- 
mal (Fox, 1974). I feel that many people who need a dog are depen- 
dent, they tend to be other-directed, and they gam considerable 
emoHonal saHsfaction from having a depndent compamon m theu 
Uves. However, more independent, 
keep a cat in preference to a dog simply ‘ ® 
and its less demanding atdtude. The breed 
owns may be a projecHon of deeper needs and 
insecure or parLoid person may want a J 

Another person who is attempting to ve up galuja It is 

grace and agiUty may keep an A^S^an hound or a ^ 
primarily because of these reasons that the pet otten 

owner-it is something '""^^XTexperimental research and 
Against a background ^ f beginning to under- 

a scattering of clinical case luston ' ^ socialization influ- 

stand more^ompletely how domeshcariona^^so^ 

ence the behavior of man s close future relationships be- 

awareness will, I hope, not only improve 
tween pet and owner but also the relationsmp 
beings in general. 


Some may demean domesticated animals as being degenerate or in- 
ferior forms of their wild ancestors or counterparts. Others may 
see them as merely utilitarian "tools/' man-made to serve hu- 
manity, in order to satisfy and gratify our many and diverse needs. 
Yet do we fully understand our enormous obligation and debt to 
them, which is ethically far greater perhaps than our debt to wild 
forms? While the latter may be in our trust and we their stewards, 
the former are our own creations. Being so, what kind of creator are 
we, and are we to become? Our debt to them is unmeasureable, for 
we have learned and are still learning from them to become more 
fully human: responsible and compassionate. We can learn through 
them in countless ways about nature and about our own nature as 
well. If we knew everything there is to know about a hair on a dog's 
back, we would know everything about the entire world, since 
everything is interrelated in evolutionary time and global space. 

As we gain wisdom, compassion and empathy through them, 
and learn from our mistakes as they suffer for us, we may more 
surely become the creative and responsible stewards and co- 
creators of and for all life. 


Appendix I 

* » j 1 hr of Stimulation daily, comprising 
The handUng procedures consisted soundproof box with a flashing 

10 min photic stimulation in a lignt -—^fplv i sec frequency, lo nun 
light stimulus of o.i6 intensity and . anteroposterior and 5 min 

labyrinthine stimulation consisting o ^ 5^^ through an excur- 

bitemporal tUting at an Auditory stimulaflon, 2 nun each at 

sion of 45° from the horizontal, 10 of 1 o v and duration of J.o msec. 
1, 10, 10= and 10’ cycles/sec at an intensity 01 ^ jn a 
This was followed by 1 mm exposure m handling, dunng 

centrifugal rotator at approximate X 45 ty ' the Magnus, rool- 

which time a series of reflexes were reflexes (see Fox, ^9^5 

ing, righting, geotaxic, pain, P®" reflex development could be 

1966). By eliciting these reflexes, , groups. The subjects were 

assessed and compared in ir^erLd for 15 sec, dunng 

then placed in a water bath at during the first 3 wee ■ 

which time they would swim: “"wel and groomed wth a soft 

Subjects were then rubbed dty with a ha^^j^'J'^^eous stimulation «ith an 

brush for 10 min and received z mm handUng peno w 

air jet (6o°F). From 3 weeks of a^ operator. After this bandl g 

increased to include 10 min P'^X Control subjects were kept 

period, they were returned to mother, hawng fl 

under typical rearing eonditions wi* y elcaning 

scheduled human contact of ‘«^“;^“‘/„ere recorded at ' 

subjects were weighed and b®® . of the invcstiga o _ 

while the pup was lying quietly in *e h= gjobul.n and piperazine 

B weaned at 4 weeks of age, ^ 

were ' 


THE dog: its domestication and behavior 

anthelmintic and were reared singly in metabolism cages in the animal 
house environment. 

At 5 weeks of age, the subjects were tested singly in a behavior arena 
equipped with one-way windows to enable the experimenter to observe 
the animals without being seen. The arena contained cloth bedding from 
the mother of the pups and, in another corner, a brightly colored child's 
toy. The reactions of the subjects were observed for 5 min when they were 
first placed in the arena, and the observations continued for 5 min more 
after these objects had been removed. The subjects were then replaced for 
5 min more of observation. The observers with stopwatches indepen- 
dently recorded the duration of certain activities of each pup throughout 
each of the three 5-inin observation periods, and time scores were then 
averaged for each group. The activities observed and time-scored were as 

1. Specific Interaction with Stimulus. Duration of interaction with either 
cloth or toy, including approach, play, chewing, licking, carrying, and 
lying beside or running around the object, was recorded. 

2. Nonspedfic Exploratory Activity. The time spent exploring the arena 
was recorded, including sniffing and Ucking walls and floor and jumping 
up at walls, looking up at walls (visual), and attention to extraneous noises 
(air conditioner turned on as sound blanket). During this activity period, 
pup never approached cloth or toy. 

3. Random Activity. The time spent sitting or pacing the arena without 
any overt reaction to cloth or toy or attention toward walls, floor, or ex- 
traneous noises was recorded. 

4. Distress Vocalization. As a level of emotional arousal, the number of 
distressful yelps and the duration of distress vocalization was recorded by 
one observer only while the other observer noted what else the pup was 
doing (random or nonspedfic exploratory activities). There was a high 
correlation between distress vocalization and nonspecific exploratory ac- 

After this 15-min testing period, the subject's approach to a passive 
observer in the arena was determined, and then approach and following 
response were assessed while the observer walked around the arena. The 
ability of the pup to negotiate a simple wire-mesh barrier placed between 
him and the observer was next used to assess detour behavior. Four trials 
were allowed, and if the subject was able to come around the barrier to the 
observer one end was blocked; if there was an end preference, the preferred 
side was blocked first. The time taken to pass around the barrier and the 
number of trials required were recorded. Finally, the social interaction of 
these differentially reared subjects was observed when they were placed 
together in the arena, which still contained the cloth and toy. After 5 min 

Appendix I 


of observation, the experimenter entered the arena and observed the ef- 
fects of the presence of a human on the group behavior of the pups. After 
these behavior observations, EEG recordings were taken on a Grass 
6-channel recorder or on an Offner 8-channel type R dynograph, EEG 
recordings were also taken and evoked responses to visual and auditoiy 
stimuli of various frequencies were recorded on a computer of average 
transients (CAT 400 B) and monitored on an osdlloscope via a Grass 
6-channel EEG recorder. Recordings were taken while the subjects were 
lying quietly awake and also while they were asleep in a darkened room; 
they were retained in a copper-gauze box lined with foam rubber. Selected 
subjects were then killed and several organs were dissected in the cold 
room at 37“F. The brain was dissected for histological examination, and 
the adrenal glands were dissected and prepared for epinephrine and 
norepinephrine analysis. Some tissues were also prepared for lipid 

Appendix II 


interval. (9) Finally the heart rate change following a 5-sec duration bell (75 
dB) placed outside the plywood arena next to the comer where the cub 
was lying is recorded. 


This study is based on the notion that confinement in a holding cage 
would be stressful and that cubs might react to such stress differently 
because of individual differences in emotional reactivity (which correlate 
with sodal rank). Blood samples were taken at arbitrarily selKted 
for plasma corticosteroid analysis with the anticipation t at in ^ 
differences in the intensity and duration of the stress . * 

found. Six cubs from the two litters, selected on the basis o 1° 

mnk scores, were each placed in a a x aVr X aVr ft 
had been cleaned with Pinesol and lined with hay. e ^ 
placed in a dimly Ut and relatively soundproof room OnV/'™ 

used for each run, 4 « of „ ‘"f.j^^TtresTwas kept to a minimum 
and 60 min after cordinement. Handbng s accessible and 

while these samples were being taken, The hair over each foreleg 

the entire procedure taking no more ^ the EKG study in 

had been shaved the previous day Twenty-four hours after 

order to minimize additional handlmg , .ccBM andRcBrd of Litter 
these samples had been taken, four of the cubs (ScB d 
I and ScBld and BIUc 2 of Utter II) were '"icc^ at the same 

the time of confinement, and blood samp es k, attempt to elicit 
intervals. The rationale behind this latter ‘ccatment^^as 
a maximal plasma corticosteroid response, ihreshold and re- 

the earlier samples, '"f’“^°"and duration might be disclosed 

sponse magnitude as well as latency 


THE dog: rrs domestication and behavior 

min duration were run on alternate days for 8 days. As reported earlier 
(Fox, 1972a), this test is of value in identifying the most dominant and 
subordinate cubs. Middle-ranking cubs of Utter I, which showed greater 
proximity tolerance and "shifting" or relative dominance (in that one 
member of a pair appears to be dominant while in possession of food), 
were impossible to rank in a linear hierarchy. This test was most valuable 
in identifying the highest and lowest ranking cubs for later physiological 
tests. For this dominance test, and for the evaluation of fear reactions and 
exploratory behavior when presented with a novel stimulus, the same 
ratings as detailed earlier (Fox, 1972a) were used. 


Using the same horizontal stimulus as developed earlier (a 30 cm x 2 m board 
with a 30-cm black square centered by a lo-cm white cross. Fox, 1972), the 
latency of response or emergence time from the nest box was recorded for 
each cub. 



THE dog: its domestication and behavior 

week for approximately 15 min for making growth measurements. They 
were therefore essentially unsodalizcd but used to handling, during 
which they would manifest passive submission, occasional defensive ag- 
gression, and would attempt to escape whenever possible. All cubs 
showed the flight reaction when approached, and only the two highest 
ranking cubs would approach a passive person in the home cage to within 
a distance of 4-6 ft; none made contact or showed active submissive greet- 
ing. All cubs had received the same handling and no preferential treat- 
ment prior to the time of testing. 

Appendix III 


wooden guillotine door was a start-box 26 in. square and 18 in. high. The 
connecting door was 19 in. wide and 20 in. high. The start-box had a 
hinged top which was fastened down by a screen door-type latch. The 
arena was lighted by four 400-watt fluorescent tubes so as to light the 
center square with 145 foot candles. The start-box was not lighted. When 
the door to the start-box was opened and the lid raised, the lighting level 
in the box was 5 foot candles. The ceiling of the arena was 7^2 feet from the 
floor. Observation was made through two one-way mirrors. One was in a 
corner by the start-box, and the other was directly opposite it. Both win- 
dows were 46 in. above the floor, high enough to prevent the puppies 
from seeing their reflection. Directly opposite the start-box erUrance to t c 
arena, a turntable was mounted with its base to the wal . . ^ 

was painted red and white. A table tennis ball and a tennis a 
suspended by a light chain from the top of the turntable m a 
that, when revoMng, the turntable hit the balls and caused them to 
bounce and the chains to emit a clanging sound. The turn able was set to 
78 rpm. TTris apparatus is hereafter refened to as revo^tng stunulus^ 
Below the turntable was a box constructed so that 8 

recorder could be placed in it from °“*«de t dynes/cm’) at the 

ted a variety of noise levels ranging up to 8o dB ( • j ^ , 

start-box aLa interface. The frequendes ran^ 

sound was constructed so as to vary ^ “1 .. uf the 

loudness in a random manner. In the ® ^ j 5 ^^d a foot above the 

box entrance and to the left of 'h® ,he rag st.mulus 

floor was mounted an apparatus hereafter , „gs was cotton 

It consisted of a cylinder wrapped with rag . hopefully, an 

rope tied so that loose ends dangled in the air m what was, pc 

entidng manner for the puppy. recorded on Cramer timers 

The time spent in the box ^punted on the wall to lx- 

which timed to the nearest .01 mm. Ti 
read outside each observation window. 


THE dog: its domestication and behavior 

water and dry food ad Ubidum. In addition, a canned food and vitamin-min- 
eral mix were fed to the puppies twice daily. On days with good weather and 
on which the puppy was not being tested, it was put out into a large wooded 
area with other puppies its size and allowed to explore and to play for 
approximately 5 hr. Water and dry food were available at all times in these 
areas. Up to 30 puppies were toglher at one time. This procedure was 
followed until the puppies were 10 months old. 

Starting on the 21st day of age the puppies were played with and 
handled in litters at least twice a week for at least 15 min each session. At 
weaning each pup was assigned to an individual handler. The puppies 
continued to be handled twice a week. They were walked on a leash and 
exposed to many different situations and environments such as au- 
tomobiles, cats, rabbits, woods, and a lake. In addition, each pup was 
encouraged to “rough-house" with its handler, to play fetch, and to pull at 
a rag. Once each week each puppy was subjected to a formal evaluation 
session during which it underwent a battery of tests including “come" and 
“sit" commands, fetch, rag play, and a maze on the 8th, 9th, and nth 

At least once each week the puppies and their handlers chased a man 
(decoy) who was trailing a rag. The puppy was encouraged to bite the rag 
and to pull on it. There was generally a heightened sense of excitement in 
all of the puppies observing as well as the puppy doing the actual chasing. 
By 12 weeks of age most puppies were vigorously pursuing the decoy and 
biting the trailing rag. As the game progressed and the puppy matured, 
the rag was changed to a wrapping of cloth around the decoy's arm. 

To summarize the puppies' experiences prior to novel experience test- 
ing, they were kennel raised, exposed to a large variety of situations, had 
been taught to be somewhat aggressive with humans, had never been 
scolded Of treated harshly, and had been well socialized with humans and 
other puppies their size. Every effort had been made to prevent a stable 
status order from developing with cage mates. If there was an obvious 
dominance hierarchy developing within a pen, the pups in that pen were 
separated and put into the other pens. 

Novel Situation Apparatus 

The novel situation apparatus was an 8i-in. square room which had 
the floor marked into nine 26 in. squares separated by 3/4-inch black tape. 
The floor was painted gray and the walls were an off-white. Adjacent to 
the room, hereafter called the arena, and connected directly to it by a solid 

Appendix III 


Urination and defecation while undergoing the novel experience test 
was rare and subjectively appeared to be unrelated to the activity level or 
distress vocalizations of the puppies. Whenever elimination did occu^ 
prior to the next puppy's session, the area was scrubbed and deodo^ed 
with a disinfectant solution. No sanitization procedures were u ' ' e e 
tween sessions of most other puppies. 

Obtained blood samples were centrifuged and the day's plasma col- 
lection sent to the laboratory for analysis. The EKG recordings were rea or 
heart rate by counting the QRS spikes per unit of time. 


Each puppy was evaluated continuously from birth. If a 
nature" as hip dysplasia, 

peramental character such as shyness, tear • as a breeder 

appeared, the dog was eUminated ^ "og^Actual evaluaHon after 
and, if the condiHon was severe, as a | who were looking 

the 12th week of age was done by expenen p it may come 

for a stable dog which could adapt lo^cally 0 ^ ijeals for a 

across. Adapt means perform according o rurious, aggressive 

given situation. Generally the ‘•“S threshold, a high pain 

only when appropriate, have a h'g evaluator gave pass/fail 

threshold, and show no fear in new siWa ' j|ed as to the future use 
scores to all dogs at the time the deasion w ^ degrees o( 

of each dog. The score was on a scaleo } o ° , .j |i,e 3 to o scores 

success and 1 and o being degrees of fm • ee appropriate. If. at J 

will appear throughout the results an ■ ^ en evaluation 

year of age, prior disposition had not been mad^eoHhe_^p&^_^^.„, 

score was also rendered on the basis o 


THE dog: its domestication and behavior 

cortisol/loo ml plasma. Accuraqr calculated as the standard deviation of 
percent recovery for 0.4 /xg cortisoliioo ml plasma added as internal stan- 
dard was found to be 93 ± 21%. The analysis was performed by the Army 
Environmental Hygiene Agency at Edgewood Arsenal, Maryland. 


Not later than the day prior to testing, the hair was clipped over the left 
jugular vein and the right and left fifth and sixth intercostal spaces at the 
level of the elbow. 

When the apparatus had been set up and tested the puppy was car- 
ried into the testing area and placed on a metal table. The puppy was 
positioned for bleeding from the jugular vein in such a manner as to place 
minimal stress on the puppy yet aid speed and ease of collection. The 
blood was collected in a heparinized 6-cc syringe with a 21-gauge iVa-in. 
needle. If the collection procedure was not an immediate success with a 
minimal amount of struggling by the puppy, that particular sampling at- 
tempt was immediately terminated. After collection of this baseline sam- 
ple, the puppy was placed in the biotelemetry harness and the electrodes 
secured. The baseline heart rate was then obtained while the puppy was 
minimally restrained on the table top. The telemetered EKG was recorded 
for a 0.4-min period. Electrode connections and the telemetry apparatus 
were observed for proper functioning while recording the heart rate. The 
puppy was then immediately placed in the box and the lid secured. The 
puppy was left in the box for i min. Heart rate was recorded during the 
first and last 0.4-min periods while in the start-box. While the puppy was 
in the start-box the arena noise, turntable, and lights were turned on. 
After 1 min the guillotine door to the arena was raised and locked open. 
Four different EKG recordings were made during the 3 min the puppy was 
in or had access to the arena. The recordings were each 0.4 min long and 
were evenly spaced throughout the 3-min session. At the termination of 
the 3-min session, the puppy was called back and removed from the box. 
Two minutes following termination of the lest the heart rale was again 
recorded as in the baseline. At the 5-min mark after termination of the 
arena testing, another heparinized blood sample was obtained from the 
jugular following the same procedure used in obtaining the baseline sam- 
ple. The puppy had been restrained on the table top from removal from 
the box to the time of the 5-min blood collection. After that collection it 
was placed alone in a large pen adjacent to the testing area. Approximately 
14 min following termination of the novel experience test, the puppy was 
retrieved from the pen and blood was collected at the 15-min mark. 


Abies, E. D. (1969). Home-range studies of red foxes (Tulpis P 

Mamm. 50, 108-120. . ^ ,,968) Cardiovascular changes 

Adams, D. B., Bacelli, G., and Maiiaa, G. (l^h 1239- 

during preparation for figftting behavio 

- I r.^intnj VV. B. Saundcrs Co.. 
AUee, W. C. (1949). Principles of Animal tcoo^- 

Philadelphia. . »he adrenal 

Andrews, R. V. (1968). 

metabolism of the brown lemming, y ^ behavior in nun and 

Astrup, C. (1968). Pavlovian Bdiaviorm Aramab 

animal. Pages 117-128 in M. W. Fox (E 

W. B. Saunders. Philadelphia. ^ laboratoO' 

Barnett, S. A. (1958). Experiments on "Neop o la 

rats. Brit. J. Psych. 49, 195-20E „puu.) 

Barnett. S. A. and Stoddart, R- ' cq 321-326. 

on conflict among wild rats. /- ■ ' j^-ejopment of 

Bateson, P.P.G. (1969). Imprinting and Ih £.v/y '■.-'•‘r 

Pages 109-124 in A. Ambr<»c (to-t. 

Academic Press, New York. 109-124- PnArrnual 

Beach, F. A. and LeBoeuf, B. (1%7)- yg. 558 . 

mating in the bitch. Anim. Bchau. • 



Candland, D. K., Taylor, D. B., Dresdale, L., Leiphart, J. M., and Solow, 
S. P. (1969). Heart rate, aggression and dominance in the domestic 
chicken. /. Comp. Physiol. Psychol. S7, 70-76. 

Candland, D. K., Bryan, D. C, Nazar, B. L., Kopf, K. J. and Sendor, M. 
(1970). Squirrel monkey heart rate during formation of status orders, j. 
Comp. Physiol. Psychol. 70, 417-423. 

Cannon, W. B. (1956). "Voodoo" death. Psychosom. Med. 19, 182-190. 
Chance, M. R. A. (1962). An interpretation of some agomshc 
role of "cut-off" acts and postures. Symp. Zool. Soc. on . , 

Chess, S. (1969). Introduction to Child Psychiatry. Grune & Stratton, New 

ChiareUi, A. B. (1975). The chromosomes of 

W. Fox (Ed.), The Wild Canids. Van Noshand Remhold, New YorK 

• fVip pxMvations of Ihc 

Qutton-Brock, J. (1969). Cami''“f , G W Dimbleby (Eds.), nr 

Jericho TeU. Pages 337-^5 inP.J.UAo an.^. - ^ ^ London. 

Domestication and Exploitation of Animals. VuO. i„,jnancc:a 

Corbett, L. and Newsome, A. (1975). fEd ) Vie Wild Onids. 

preUminary analysis. Pages 369^79. n M. W. Fox (Ed.), 

Van Nostrand Reinhold, New York. ^ ^ (1975). Pel- 

Corson, S. A., O'Leary Corson, ^^nderson (Ed.),Prt 

facilitated psychotherapy. . 

mats and Society. Balliere Tindall, on 

Crisler, L. (1958). Arctic Wild. Harper Brothers, ^ ,\p- 

Darwin, C. (1873). The Expression cf the Emotions m Man 

pleton. New York. , Plants under Domestication. 

Darwin, C. (1875). The Variation (^Animals 
2nd Ed. John Murray, London. ^rnusal i^ature 211' 

Dehus, J. D. (1967). Displacement acdvities and 

1259-1260. . ,,Hnn input and cmooorul 

Denenberg,V.H. (1964). Critical pen^^59mu^^,^^^^^, 7,,351-a--^ 

reactivity: A theory of infantile stim „n,o6onal reacu^ty and 

Denenberg, V. H. (1967). Shmulabon mjNang.^ 
exploratory behavior. In . University 

Neurophysiology and Emotion. Rockefe ^-ongeneuc transirax-i " 

Denenberg, V. H. and Rosenberg, K- * 
of information. Nature 216, 549. 


THE dog: rrs domestication and behavior 

Beck, A. M. (1971). The life and times of Shag, a feral dog in Baltimore. 

Natural Histoty 80 (8), 58-65 (October). 

Beck, A. M. (1973). The Ecology of Stray Dogs: A Study of Free-ranging Urban 
Animals. York Press, Baltimore. 98 pp. 

Bekoff, M. (1972). An ethological study of the development of social in- 
teraction in the genus Canis — A dyadic analysis. Ph.D. Dissertation, 
Washington University, St. Louis, Missouri. 

Belkin, D. A. (1968). Bradycardia in response to threat. Amer. Zool. 8, 775 

Bennett, E. L., Diamond, M. C., Rosenzweig, M. R., and Krech, D. (1964). 
Chemical and anatomical plasticity of the brain. Science 146, 610-619. 

Berkson, G. (1968). Development of abnormal stereotyped behaviors. De- 
velop. Psychobiol 1, 118-132. 

Berry, R. J. (1969). The genetical implications of domestication in animals. 
Pages 207-217 in P. J. Ucko and G. W. Dimbleby (Eds.), The Domestica- 
tion and Exploitation of Animals. Duckworth & Co., London. 

Beylaev, D, K. and Trut, L. N, (1975). Some genetic and endocrine effects 
of selection for domestication in silver foxes. Pages 416-426 in M. W. Fox 
(Ed.), 77ie Wild Canids. Van Nostrand Reinhold, New York. 

Blauvelt, H. (1964). The physiological analysis of aggressive behavior 
(died personal communication by D. E. Davis). Pages 53-74 m W. Etkin 
(Ed.), Social Behavior and Organization Among Vertebrates. University of 
Chicago Press, Chicago. 

Blcichcr, N. (1963). Physical and behavioral analysis of dog vocalizations. 
Am. J. Vet. Res. 24, 415-427. 

Bldcher, N. Personal communication. Downstalc Medical Center, Stale 
University of New York, New York. 

Blizard, D. A. (1971). Individual differences in autonomic responsivity in 
the adult rat. Psy^toso/n. Med. 33, 445-457. 

Bowlby, J. (1953). Some pathological processes set in train by early 
mother-child separation. J. Mait. Sci. 99, 265-272. 

Bowlby, J. (1971). Attachmait. Penguin, London. 

Dmnncr, F. (1968). The application of behavior studies in small animal 
practice. Pages 398-449 in M. W. Fox (Ed.), Abnormal Bdtavior in Animals. 
\V. D. Saunders, Philadelphia. 

Burrows, R. (1968). Wild Fax. David & Charles, Newton Abbot, England. 



Fox, M. W. (1969b). The anatomy of 

Canidae: a developmental and comparative study. Behmour 35, 


Fox, M. W. (1970a). A comparative study of !. 

expressions in canids: wolf, coyote and foxes. Behmour 37, 4V 

Fox, M. W. (1970b). Neurobehavioral deveiopmenUnd the geno 

ronment interaction. Quart. Rev. Biol., 45, 

Fox, M. W. (1971a). Integrative Development of Brain and Behmor ^n og. 
University of Chicago Press, Chicago. Tnnathon 

Cape, London. ,i:Hnns on the behavior of labora- 

Fox, M. W. (1971c). Effects of ^“""8 , So Defining the laboratory 

tory animals. Pages 294-012 m Nat. Acad. t>a. 

Animal. Washington, D.C. hIp and sodo-sexual signals 

Fox, M. W. (1971d). Ontogeny of sodo-mfanble and 
in canids. Z. Tierpsychol. 28, 185-2iu- individual differences 

Fox, M. W. (1972a). Sodo-ecologjml topUmtio^ perspective. Behmour 
in wolf Utters; a developmental ana e 

41, 298-313. , McCann, New York. 

Fox, M. W. (1972b). Understanding Your Dog- 

(Blond & Briggs, London. 1974.) Behaviour 

Fox, M. W. (1973). Sodal dynamics of three ca 

47, 290^01. vmir 0,1 coward. McOnn. New York. 

Fox, M. W. (1974). UnderstandmYm 

(Blond&Briggs, London. 1974.) ^ ^ canids. Pag“ 

Fox, M. W. (1975a). Evolution 

in M. W. Fox (Ed.), The Wild Canids. Behavior- U 

Fox, M. W. (1975b) Concepts 

versity of Minnesota Press, Mmnesota. ^ ^ Anderson 

Fox, M. W. (1975c). Tet-^^ B^er^Tind^aU, caiuidm 

(Ed.), Pet Animals and Soaety- Toronto 

Fox, M. W. (1976). The needs of people for S „et.c . 

Symposium on Pets and Soaety, 

Fox, M. W. (1978). fn Search of Wildness a W 

tion. „ V (1973).Phy-“'‘>P“'-'' 

Fox, M. W. and Andrews, K. *■ ' 


THE dog: its domestication and behavior . 

Denenberg, V. H. and Whimbey, A. C. (1963). Infantile stimulation and 
animal husbandry; A methodological study. }. Comp. Physiol. Psychol. 
56, 877-878. 

Eibl-Eibesfeldt, I. (1970). Ethology: The Biology of Behavior. Holt, Rinehart & 
Winston, New York. 

Eisenberg, J. and Leyhausen, P. (1972). The phylogenesis of predatory 
behavior in mammals. Z. Tierpsydtol. 30, 59-93. 

Ely, F. and Peterson, W. E. (1941). Factors involved in the ejection of milk. 
/. Dairy Sd. 24, 211-233. 

Enders, R. K. (1945). Induced changes in the breeding habits of foxes. 
Sodometry 8, 53-55. 

Engel, G. L. (1950). Fainting. Charles C. Thomas, Springfield, Illinois. 
Epstein, H. (1971). The Origin of the Domesticated Animals of Africa. Afiicana 
Publishing Corp., London. 

Ewer, R, F. (1973). The Carnivores. Cornell University Press, Ithaca, New 

Far4 and Catlett (1971). Cardiac response and social behavior in guinea 
pig. Anim. Behav. 19, 514-523. 

Fox, M. W. (1964). The ontogeny of behavior and neurologic responses of 
the dog. Anim. Behav. 12, 301-310. 

Fox, M. W, (1965). Canine Behavior. Charles C. Thomas, Springfield, Il- 

Fox, M. W. (1966). Canine Pediatrics. Charles C. Thomas, Springfield, Il- 
linois. 1966. 

Fox, M. W. (Ed.) (1968a), Abnormal Behavior in Animals. W. B. Saunders, 

Fox, M. W. (1968b). Use of the dog in behavioral research. Pages 27-80 in 
W. 1. Gay (Ed.), Methods of Animal Experimentation, Vol III. Academic 
Press, New York. 

Fox, M. W. (1968c) The influence of domestication on the behavior of 
animals. In M. W. Fox (Ed.), Abnormal Behavior in Animals. W. B. Saun- 
ders, Philadelphia. 

Fox, M. W. (1968d). Socialization, environmental factors and abnormal 
behavorial development in animals. Pages 332-355 in M. W. Fox (Ed.), 
Abnormal Behavior in Animals. W. B. Saunders, Philadelphia. 

Fox’, M. W. (1969a). Ontogeny of prey-killing behavior in Canidae. Behavior 
35, 259-272. 



Gray, A. P. (1954). Mammalian hybrids. A check-list with bibliography. 
Technical Communication 10, Comm. Agriculture Bureaux, F am 
Royal, Bucks, England. 

Guthrie, R. D. (1975). A hypothesis of density-adapted mo^hs among 
Northern canids. Pages 414^15 In M. W. Fox (Ed.), The Wild Camds. 
Van Nostrand Reinhold, New York. 

Hale, E. B. (1962). Domestication and the ^ Co^' 

Hafez (Ed.), The Behavior Domestic Animals. Williams 

Baltimore. p 

Hale, E. B. (1969). Domestication and the M 

22^ ill E. S. E. Hafez (Ed.), The Behavior of Domestic Anima 

edition. Balliere Tindall, London. n 68 74 

Harlow, H. F. (1959). Love in infant monkeys. Sd. Am. 20 , 

Hediger. (1950). Wild Animals in Captivity. 

Hediger, H. (1955). Studies of the Physiology and Behavwu 

in Zoos and Circuses. Butterworth, London. 

Henderson, N. (1970). Cerie 6 c 72 , 505-5^ 

obscured by laboratory reanng. J. Co p- y TPoroduction. 

Hill, J. L. (1974). Peromyscus: Effect of early pairmg 

Science, 186, 1042-1044. during sudden pro- 

Hofer, M. A. (1970). Cardiac and 32, 633-647. 

longed immobility in wild rodents, sy primate research 

Jensen, G. D. and Bobbitt, R. A. (1968)- J"’P''JX'serman (Ed.), Sririirr 
for understanding infant New York. 

and Psychoanalysis, Vol. 12. Grune ' „ Press, New 

Ioffe, ,. M. (1969h Prenatal Determinants cf Behavior. Pergam 

Tork. timber wolf (O'”'* 

JosUn, P. W. B. (1966). Summer A'*”“'^°>[l^°thesis, University of o- 
packs in Algonquin Park. Unpublished M.s. 

ronto. 99 pp. d the legacy of ton ' 

Keeler, C. (1970). Melanin, adrenalin, an 

81-88. , . -n color phases of the red 

Keeler, C. (1975). Genetics of behavior Q^mds. Van Nost 

fox. PagL 399-413 in M. W. Fox (Ed.), 

Reinhold, New York. coyote-dog h) n 

Kennelly, J. J. and Roberts, J. D* t 
Mammal. 50, 830-831. 


THE dog: its domestication and behavior 

correlates of individual differences in wolf litters. Behaviour XLVI, 129- 

Fox, M. W. and Bekoff, M. (1975). The behaviour of dogs. Pages 370^09 
in E. S. E. Hafez (Ed.), The Behaviour of Domesticaled Animals, 3rd edition. 
Balliere Tindall, London. 

Fox, M. W. and Clark, A. L. (1971). Ontogeny and temporal sequencing of 
agoiusdc behavior in the coyote, {Canis latrans). Z. Tierpsychol. 28, 262- 

Fox, M. W. and Cohen, J. A. (1977). Canid communication. In T. A. Sebeok 
(Ed.), How Afiimals Communicate. Indiana University Press, Blooming- 
ton, Indiana. In press. 

Fox, M. W. and Spencer, J. (1%9). Development of exploratory behavior in 
the dog: Age or experience dependent? Develop. Psychobiol. 2, 68-74. 

Fox, M. W. and Walls, S- (1973). Wild animals in captivity: Veterinarian's 
role and responsibility . }. Zoo Anim. Med. 4(3), 7-17. 

Fox, M. W., Folk, G. E., and Folk, M. (1970). Physiological differences 
between alpha and subordinate wolves in a captive sibling pack. Amer. 
Zool. 10, 487. 

Fox, M. W., Lockwood, R., and Shideler, R. (1974). Introduction studies in 
captive wolf packs. Z. Tierpsydtol. 35, 39-48. 

Funkenstein, D. H. (1955). The physiology of fear and anger. Sd, Am. 

Gantt, W. H. (1944). Experimental Basis for Neurotic Behavior. Hoeber, New 

Gantt, W. H., Newton, J. E. O., Royer, F. L., and Stephens, J. H. (1966). 
Effect of person. Cond. Reflex 1, 18-35. 

Gellhom, E. (1968). Central nervous system tuning and its implications for 
neuropsychiatry. /. Neru. & Ment. Dis. 147, 148-162. 

Gier, H. T. (1968). Coyotes in Kansas. Kansas Agricultural Experiment Sta- 
tion Bulletin 393, 1-97, 

Gier, H. T. (1975). Ecology and social behavior of the coyote. Pages 247- 
262 in M. W. Fox (Ed.), The Wild Canids. Van Nostrand Reinhold, New 

Ginsburg, B, E. (1968). Genotypic factors in the ontogeny of behavior. In J, 
H. Masserman (Ed.), Animal and Human. Grune & Stratton, New York. 

Graham, F. K. and Clifton, R. K. (1966). Heart-rate change as a component 
of the orienting response. Psychol. Bull. 65, 305-320. 



Lor^, K ( 1 ^ 0 ). Studies in Animal and Human Behavior, Vol. II. Harvard 
University Press, Cambridge, Massachusetts. 

™ Van 

nJostrand Remhold, New York. 

Lucas E. A., Powell, E. W., and Murphree, O. D. (1974). Hippocampal 
tneta m nervous pointer dogs. Physiol. & Behav. 12, 609-613. 

Lynch, J. J, (1970). Psychophysiology and development of sodai attach- 
ment. /. Nerv. & Ment. Dis. 151, 231-244. 

Lynch, j. J, and Gantt, W. H. (1968). The heart rate component of the 
sodal reflex in dogs: the conditionai effect of petting and person. Cond. 
Reflex 3, 69-80. 

Macintosh, N. W. G. (1975). The origin of the dingo; An enigma. Pages 
87-106 in M. W. Fox (Ed.), The Wild Canids. Van Nostrand, ReinhoJd, 
New York. 

Marler, P, and Hamilton, W. J-, HI. (1966). Mechanisms of Animal Behavior, 
John Wiley & Sons, New York. 

Mason, W. A. (1967). Motivational aspects of sodal responsiveness in 
young chimpanzees. Pages 12-^ in H. W. Stevenson, E. H. Hess 
and H. L, Rheingold (Eds.), Early Behavior — Comparative and Development 
tal Approaches. John Wiley & Sons, New York. 

McBride, R, L,, Klemm, W. R., and McGraw, C P. (1969). Mechanisms of 
the immobility reflex ("animal hypnosis"). Comm. Behav. Biot. 3, 33-59. 

McNab, B. K. (1963). Bioenergetics and the determination of home range 
size. Amer. Natur. 97, 133-140. 

Mech, L. D. (1970). The Wolf. Natural Histoiy Press, Neiv York. 

Meggitt, M. J. (1965). The association between Australian aborigines and 
dingoes. Pages 7-26 in A. Leeds and A. P. Vayada (Eds.), Man, Culture & 
Animals. Publ. #78, AAAS, Washington D.C 
Meier, G. W. (1961). Infantile handling and development in Siamese kit- 
tens. /. Comp. Physiol. Psychol. 54, 284-286. 

Mengel, R. M. (1971). A study of dog-coyote hybrids and implications 
concerning hybridization in Canis. /. of Mamm. 52, 316-336. 

Menzel, R. and Menzel, R. (1948). Observations on the pariah dog. Pages 
968-990m B. Vesey'PitzQerald (Ed.),The Bookof the Dog. Borden Publish- 
ing, Toronto, Canada. 

Meyer-Holzapfel, M. (1968). Abnormal behavior in zoo animats Paf;es 


THE dog: its domestication and behavior 

King, ]. A. (1968). Spedes-spediidty and early experience. Pages 42-64 m 
G. Newton and S. Levine (Eds.), Early Experience and Behavior. Qiarles 
C. Thomas, Springfield, Illinois. 

Klinghammer, E. (1967). Factors influencing choice of mate in altridal 
birds. Pages 297-303 in H. W. Stevenson, E. H. Hess, and H. L. Rhein- 
gold (Eds.), Early Behavior. Academic Press, New York. 

Kolenosky, G. B. (1971). Hybridization between a wolf and a coyote. ]. 
Matnmal. 52, 446-449. 

Kovach, J. K. and Kling, A. (1967). Mechanisms of neonate sucking be- 
havior in the kitten. Anim. Behau. 15, 91-101. 

Kummer, H. (1971) Primate Societies. Aldine, Chicago. 

Kuo, Z. Y. (1960). Studies on the basic factors in animal fighting. VII. 

Interspedes coexistence in mammals. /. Genet. Psychol. 97, 211-225. 
Kurtsin, I. T. (1968). Pavlov's concepts of experimental neurosis and ab- 
normal behavior in animals. Pages 77-106 in M. W. Fox (Ed.), Abnormal 
Behavior in Animals. W. B. Saunders, Philadelphia. 

Lacey, J. I. and Lacey, B. C. (1970). Some autonomic-central nervous sys- 
tem interrelationships. Pages 205-226 in P. Black (Ed.), Physiological Cor- 
relates of Emotion. Academic Press, New York. 

Levine, S. and Mullins R. F. (1966). Hormonal influences on brain organi- 
zation in infant rats. Science 152, 1585-1592. 

Leyhausen, P. Verhaltensstudien an Katzen. PaulParey, Berlin and Hamburg, 

Liddell, H. S. (1954). Conditioning and emotions. Scientific American 190, 

Linn, J. (1974). An evaluation of puppy heart rate and plasma cortisol 
levels as temperament predictors in German shepherd dogs. Unpub- 
lished M.Sc. thesis, Washington University, St. Louis, Missouri. 
Lockwood, R. (1976). An ethological analysis of sodal structure and affilia- 
tion in captive wolves. Unpublished Ph.D. thesis, Washington Univer- 
sity, St. Louis, Missouri. 

Long, E. M., Truex, R. C., Friedmann, K. R., Olson, A. K., and Phillips, S. 
J. (1958). Heart rate of the dog following autonomic denervation. Anat. 
Rec. 130, 73-89. 

Lorenz, K. (1966). On Aggression. Harcourt, Brace & World, New York. 

Lorenz, K. (1968). Evolution and Modification of Behavior. University of 
Chicago Press, Chicago. 



monkeys In M. W. Fox (Ed.), Abnormal Behavior in Animals. W. B. Saun- 
aers, Philadelphia, 

Sackett, G. P., Porter, M., and Holmes, H. (1965). Choice behavior in 
rnesus monkeys effect of stimulation during the first month of life 
Sciefice 147, 305-306. 

Salzen, E. A. and Comell, J. M. (1968). Self-perception and species recog- 
nition in birds. Behaviour 30, 44-65. 

Schenkel, R. {1947). Expression studies of wolves. Behaviour 1, 81-129. 

Schneirla, T. C. (1959). An evolutionary and developmental theory of 
biphasic processes underlying approach and withdrawal. Pages 1-42 in 
M. R. Jones (Ed.), Nebraska Symposium on Motivation. Nebraska Univer- 
sity Press, Lincoln, Nebraska. 

Schneirla, T. C. (1965). Aspects of stimulation and organization in 
approach/withdrawal processes underlying vertebrate behavioral de- 
velopment. Pages 1-74. in D. S. Lehrman, R. A. Hinde, and E. 5haw 
(Eds.), Advances in the Study of Animal Behavior, VoJ. I. Academic Press, 
New York. 

Scholander, P. F., Irving, L., and Grinnell, $. W. (1942) Aerobic and 
anaerobic changes in seal muscles during diving. /. Biol. Chem. 142, 

Schutz, F. (1965). Sexuelle Pragung bei Anatiden, Z. Tierpsychol. 22, 50- 

Scott, J. P. (1962). Critical periods in behavioral development. Science 
138, 949-958. 

Scott, J. P. {1968a). Evolution and domestication of the dog. Pages 243-275 
in T. Dobzhansky, M. K. Hecht and W. C. Steere (Eds.), Evolutionary 
Biology, Vol. II. Academic Press, New York. 

Scott, J. P. (1968b) Early Experience and the Organization of Behavior. Brooks' 
Cole, Belmont, California. 

Scott, J. P. (1973). Animal Behavior. Chicago: Chicago University Press. 

Scott, J. P. and FuUer. J. L. (1965). Genetics and Social Behmiar of the Dos 
University of Chicago Press, Chicago. 

Scott, M. D. and Causey, K. (1973). Ecology ol feral dogs in Alabama / 
WUdl. Mgmt. 37, 252-265. 

Silber, K. H., 

Bush R. D., and Oslapas, H. (I95S). Practical procedure for 
of corticosterone and hvdiocorh'sone. Clm. Chew. 4, 27a-2&> 


THE dog: its domestication and behavior 

476-503 in M. W. Fox (Ed-). Abnormal Behavior in Animals. W. B. Saun- 
ders, Philadelphia. 

Morton, J. R. (1968). Effects of early experience on behavior. Pages 261-262 
in M. W. Fox (Ed.), Abnormal Behavior in Animals. W. B. Saunders, 

Murphree, O. D., Dykman, R. A., and Peters, ], E. (1967). Genetically- 
determined abnormal behavior in dogs. Cond. Reflex 4, 199-205. 

Murphree, O. D., Peters, J. E., and Dykman, R. A. (1969). Behavioral 
comparisons of nervous, stable, and crossbred pointers at ages 2, 3, 6, 9 
and 12 months. Cond. Reflex 4, 20-23. 

Nesbitt, W. H. (1975). Ecology of a feral dog pack on a wildlife refuge, in 
M. W. Fox (Ed.), The V/ild Canids. Van Nostrand Reinhold, New York. 

Newton, ]. E. O. and Gantt, W. H. (1968). The history of a catatonic dog. 
Cond. Reflex 3, 45-61. 

Newton, J. E. O., Murphree, O. D., and Dykman, R. A. (1970). Sporadic 
transient atrioventricular block and slow heart rate in nervous pointer 
dogs. Cond. Reflex 5, 75-89. 

Nottebohm, F. (1970). Ontogeny of bird song. Science 167, 950-956. 

Obrist, P. A. (1968), Heart-rate and somatic motor coupling during classi- 
cal aversive conditioning in humans. J. Exp. Psychol. 11, 180-193. 

Pavlov, I. P. (1928). (Gantt, W. H., transl.) Lectures on Conditioned Reflexes. 
International Publishers, New York. 

Richter, C. P. (1954), The effects of domestication and selection on the 
behavior of the Norway rat, /. Nat. Cancer Inst. 15, 727-738. 

Richter, C. P. (1957). On the phenomenon of sudden death in arumals and 
man. Psychosom. Med. 19, 191-198. 

Riesen, A. H. (1961). Stimulation as a lequiremenl for growth and function 
in behavioral development. Pages 57-80 in D. VV. Fiske and S. R. Maddi 
(Eds.), Functions of Varied Experience. Dorsey Press, Homewood, Illinois. 

Rouget, Y. (1970). Personal communication. Department of Ethology, 
University of Rennes; film presented at International Ethology Confer- 

Royer, F. L. and Gantt, W. H. (1961). The effect of different persons on the 
heart rale of dogs. Paper presented at Eastern Psychological Association, 
Philadelphia, March 1961. 

Sackett, G. P, (1968). Abnormal behavior in laboratory-reared rhesus 



monkey calls under normal conditions and under acoustic isolation. 
Behaviour XLVJI, Part 3^, 230-239, 

Wolf, S. (1964). The bradycardia of the dive reflex — a possible mechanism 
of sudden death. Trans. Amer. Clin. Climat. Ass., 192-200. 

Woolpy, J. H. Socialization of wolves. Pages 82-94 in J. H- Masserman 
(Ed.), Animal & Human. Grune & Stratton, New York. 

Woolpy, J, H. and Ginsburg, B. E, (1967), Wolf sodalization: a study of 
temperament in a wild social s^pedes. Amer. Zool. 1, 357-364. 

Zeuner, F, E. A History of Domesticated Animals. (1963), Harper iSc Row, 
New York. 

Zimen, E. (1971). Wol/e und Konigspudel, In W, Wickler (Ed,), Ethol. 
Studien. Piper Verlag, Munchen, 


THE dog: its domestication and behavior 

Silver, H. and Silver, W, T. (1969). Growth and behavior of the coyote-like 
canid of Northern New England with observations on canid hybrids. 
Wildlife Monographs 17, 1-41. 

Spitz, R. (1949). The role of ecological factors in emotional development. 
Child Development 20, 145-155. 

Spitz, R. (1950) . Anxiety in infancy: a study of its manifestations in the first 
year of life. Int. J. Psychoatial. 31, 138-143. 

Staines, H. J. (1975). Distribution and taxonomy of the Canidae. Pages 3-26 
in M. W. Fox (Ed.), The Wild Canids. Van Nostrand Reinhold, New York. 

Tembrock, G. (1958). Lautenwiclung bein fuchs; sichter gemacht. 
Umschau, 58, 566. 

Tembrock, G. (1960). Spezifische laulformen beim rotfuchs (vulpes vul- 
pes) und ihre beziehunger zum verhalten. Saugertierkundl. Mitt 8, 150- 

Tembrock., G. (1968). Land mammals. Pages 338-404 in T. A. Sebeok 
(Ed.), Animal Communication. Indiana Unversity Press, Bloomington, In- 

Theberge, J. B. and Falls, J. B. (1967). Howling as a means of communica- 
tion in wolves, Amer. Zool. 7, 331-338. 

Thomas, A., Chess, S., and Birch, H, G. (1970). The origin of personality. 
Sci. Amer. 223, 102-109. 

Thompson, W. R. (1957). Influence of prenatal maternal anxiety on emo- 
tional reactivity in young rats. Science 125, 698-699. 

Trumler, E. (1973) Your Dog and You. Seabury, New York. 1973. 
Vandenberg, J. G. (1969). Male odor accelerates female sexual maturation 
in mice. Endocrinology 84, 658-660. 

Van Lawick, H. and Van Lawick Goodall, J. (1971). ITie Innocent Killers. 
Houghton Mifflin, New York. 

Vauk, G. (1953) Die abwandlung der Beutefanghandlung des hundes im 
zuge der domestikation. Zool. Anzeiger (Deutsche Zoologische Geselscaft), 
Supplement 17, 180-184. 

Volgyesi, F. A. (1966). Hypnosis of Man and AnUnal. Ballifere, London. 

Wallace, R. K. and Benson, H, (1972) The physiology of meditation. Sci. 
Amer. 226, 84-90. 

Weber, E. and Weber, E. H. (1845). Gled in Long et al. (1958). 

W'mter, P., Handley, P. Ploog, D. and Schott. (1973). Ontogeny of squirrel 


Abies, E. D., 51 
Abnormal behavior, 237, 259 
Activity, feral dogs, 48 
Adams, D. B., 178 
Adaptive radiation, 7 
Adrenals and stress, 202 
A-elidting sounds, 84 
Affection and physiology/ 231 
Aggression, development of, 33 ^ 
displays, 98, 99; and prey killing, 
130; and sex, 147, 149 
AUee, W. C., 4 
Ancestry, dog, 242 
Andrews, R. V., 269 
Astrup, C., 226 
Attachment. See socialization 
Attention bradycardia, 179 
Autonomic balance, 226 
Autonomic tuning, 165 

Barks, 76, 87 
Bamclt, S. A., 15, j6, 18 
Bateson, P. P. G., 172 
Beach, F. A.. 37 

-k, A. M., 65 

savior, development, .55: ^ 
,me 5 tication, 8 , 25 o;ofh)‘’"'^*' 

coff, M., 9 > 

kin, D. A., ^ 77 ; -“5 

melt. E. L., 166, 169 
■kson, G.. 188 

TV, R- ^9 

6, 127 

uvelt, H-, 133 

ichcr, N-. 7-’ "5 

^rd, D A . 190 

,d, scxuJl, 28 

Wby. J . '?;* ...4 

dvcjrdu ' 


in 2nd vnvnvnn-.n . 
cd diift-vcnco. 3 , 

..duTg J j 

•ding. ‘ jr-! 




Environment, deprivation, 166; 
and development, 171 
Environmental influences, 153 
Environmental input, 175 
Epstein, H., 242, 243 
Ergotropic tuning, 205 
Estrus, 37; hybrids, 102 
Ethogram, 239 
Ethostasis, 232 

Evolution of submission, 229 
Ewer, R. F., 130 

Fara, G., 178 
Fear bradycardia, 177 
Fear of strangers, 38 
Feral dogs, 41; activity of, 41 
Flight distance, 11, 216 
Food and sociability, 243 
Forelimb stab action, 123 
Fox, M. W., 8, 14, 16, 24, 28, 32, 
36, 41, 66, 69, 70, 77, 85, 87, 95/ 
97/ 99/ 102, 104, 105/ ^^ 7 ' 

13O/ 135/ 154/ 158/ 161, 164, 167, 
171, 198, 200, 203, 218, 23I/ 235, 
238, 250, 259, 261 
Funkenstein, D. H,, 207 

Gantt, W. H., 182 
Gellhom, E., 178, 205, 208, 222, 

Genetics, of behavior, 91; and 
domestication, 238; and envi- 
ronment, 169; and handling, 164; 
and heart rate, 227 
"Gentling," 162 
Gier, H. T., 28, 104 
Ginsburg, B. E., 164, 171, 195 
Graham, F. K., 181, 228 
Gray, A. P., 36 
Grooming, effects, 162 
Grunts, 77 
Guthrie, R. D., 237 

Hale, E. B., 3, 5, 14, 15/ 16, 17/ 18 
Handler, reactions to, 142 
Handling, and domestication, 165; 

effects, 163; in pups, 192 
Handling responsiveness, 102 
Handling stress, 189; in dogs, 164 
Harlow, H. F., 184 
Heart rate, development, 184; and 
early experience, 189; and tem- 
perament, 34, 187, 196, 209 
"Heck's law," 237 
Hediger, H., 150, 157, 216 
Henderson, N., 169 
HiU, ]. L., 170 
Hofer, M. A., 177/ 228 
Home range movements, 51 
Howls, 77 

Hunting behavior, 61, 107 
Hunting, breed differences, 129 
Hybridization, 17 
Hybrids, and prey kiUing, 107; 
specific actions, 123 

Imprinting, 158 
Inbreeding problems, 257 

fandlism, 151 
euinal response, 102 
heritance, non-genehc, 171 

;n, G. D., 168 
, J. M., 186, 19° 

r, C., 16, 237 
elly, J- J - 
g of prey, 107 
J. A., 17= 

hammer, E , 150, 1S7 

Kovach, J. K , 17* 
Kummer, H , 3b 


THE dog: its domestication and behavior 

Brunner, F., 259 
Burrows, R., 28, 123 

Candland, D. K., 34, 204, 206 
Canids, distribution, 22; social or- 
ganization, 26, 28; taxonomy, 23 
Cannon, W. B., 225 
Cardiac activity, 177 
Chance, M. R. A., 224, 231 
Chess, S., 161 
ChiarelU, A. B., 242 
Clutton-Brock, J., 249 
Coat color and temperament, 16, 

Coat type, hybrids, 95 
Communication, in canids, 24; 
vocal, 69 

CompatabUity, interspecies, 137 
Conditioning and heart rate, 182 
Contactual comfort, 183 
Coos, 77 

Corbett, L., 39, 150 

Corson, S. A., 259 

Coyote X dog hybrid, 91 

Crisler, L., 74 

Critical distance, 216 

Critical period, socialization, 160 

Critical periods, 171 

Darwin, C., 85 
Degeneration, 240, 258 
Delius, J. D., 229 
Denenberg, V. H., 162, 163, 171, 
172, 179, 189, 190, 195 
Dependence, 253 
Deprivation, environmental, 166 
Destabilization, 19 
Development, heart rate, 184; 
stages of, 153; vocal, 80 
Deviant behavior, 17 
Dingo, 241, 249 

Disease susceptibility, 225 
Disinhibition of bite, 129 
Displays, and domestication, 236; 
and heart rate, 230 
Diving reflex, 178 
Docility, 8 

Dog X coyote hybrids, 91 
Dog, domestication, 37; origins, 


Dogs, feral, 41 

Domestication, behavior effects, 

8; comparisons, 37; environmen- 
tal influences, 153; history of, 5; 
and hunting, 129; and in- 
terspecies interactions, 138; 
physiological effects, 18; predis- 
posing factors, 9; and prey catch- 
ing, 107; stages of, 5; and sympa- 
thetic tone, 222; and vocaliza- 
tions, 69 

Dominance and heart rate, 198, 

Early experience, 162; and play, 

Early rearing patterns, 158 
Ecology, and behavior, 26; feral 
dogs, 41 

Economic charactercstics, 8 
Ectomorph, 93, 95 
EEG development, 155 
Eibl-Eibesfeldt, I., 14 
Eisenberg, J., 109 
Ely, F., 15 

Empathy and heart rate, 232 
Emotional development, 175 
Emotional disorders, 161, 259 
Emotions and heart rate, 177 
Enders, R, K., 11 
Endomorph, 95 
Engel, G. L., 178 
Enrichment, environmental, 166 


Environment, deprivation, 166; 
and development, 171 
Environmental influences, 153 
Environmental input, 175 
Epstein, H., 242, 243 
Ergotropic tuning, 205 
Estrus, 37; hybrids, 102 
Ethogram, 239 
Ethostasis, 232 
Evolution of submission, 229 
Ewer, R. F., 130 

Fara, G., 378 
Fear bradycardia, 177 
Fear of strangers, 38 
Feral dogs, 41; activity of, 41 
Flight distance, 11, 2x6 
Food and sociability, 243 
Forelimb stab action, 123 
Fox, M. W., 8, 14, 16, 24, 28, 32, 
36, 41, 66, 69, 70, 77, 85, 87, 95, 
97/ 99/ ^02, 104, 105, 107, 109, 126, 
130, 135, 154, 158, 361, 164, 167, 
171, 198, 200, 203, 2x8, 231, 235, 
238, 250, 259, 261 
Funkenstein, D. H., 207 

Gantt, W. H., 182 
Gellhorn, E., 178, 205, 208, 222, 

Genetics, of behavior, 91; and 
domestication, 238; and envi- 
ronment, 169; and handling, 164; 
and heart rate, 227 
"Gentling," 162 
Gier, H. T., 28, 104 
Ginsburg, B. E., 164, 171, 395 
Graham, F. K., 181, 228 
Gray, A. P., 36 
Grooming, effects, 162 
Grunts, 77 
Guthrie, R. D., 237 


Hale, E. B., 3, 5, 14, 15, 16, 17, 18 
Handler, reactions to, 142 
Handling, and domestication, 165; 

effects, 163; in pups, 192 
Handling responsiveness, X02 
Handling stress, 189; in dogs, 164 
Harlow, H. F., 184 
Heart rate, development, 184; and 
early experience, 189; and tem- 
perament, 34, 187, 196, 209 
"Heck's law," 237 
Hediger, H., 150, 157, 216 
Henderson, N., 169 
Hill, J. L., 170 
Hofer, M. A., 177, 228 
Home range movements, 51 
Howls, 77 

Hunting behavior, 61, 107 
Hunting, breed differences, 129 
Hybridization, 17 
Hybrids, and prey killing, 107; 
specUic actions, 123 

Imprinting, 156 
Inbreeding problems, 257 
Infantilism, 353 
Inguinal response, 102 
Inheritance, non-genetic, 171 
Interspedes play, 133 

Jensen, G. D., 168 
Joffe, J. M., 165, 166, 190 
Joslin, P. W. B., 72 

Keeler, C., 16, 237 
Kennelly, J. ]•> 3^4 
KiUing of prey, 107 
King, }. A-, 172 

KHnghammer, E.. 150, i 57 
Kolenosky, G. B.. 36 
Kovach, /• K ' ^72 
Kummer, H.. 36 


the dog: its domestication and behavior 

Kurtsin, I. T., 179, 205, 222, 225, 

Lacey, J. L, 179, 180, 181, 189, 204, 
205, 218, 228, 229 
Leadership, 52 
Leap-stab action, 123 
Levine, S., 163, 174, 189 
Leyhausen, P., 123, 224, 226 
Licking, social, 102 
Liddell, H. S., 183 
Linn, J., 208, 209 
Lockwood, R., 237 
Long, E. M., 177 
Lorenz, K., 16, 157, 251 
Lucas, E. A., 228 
Lynch, J. J., 182, 183, 184, 204, 205 

Macintosh, N. W. G., 24, 249 
Man-dog relations, 257 
Marler, P., 25 
Mason, W. A., 168 
Marking behavior, 52 
McBride, R. L., 221 
NcNab, B. K., 51 
Mech, L. D., 29 
Meggitt, M. J., 241 
Meier, G. W., 164, 194 
Mengel, R. M., 91, 104 
Menzel, R., 245, 247, 251 
Mesomorph, 95 
Metacommumcation, 66 
Mews, 77 

Meyer-Holzapfel, M., 168, 172 
Mimicry, 236 
Mixed sounds, 77 
Monogamy, 37 
Morning greeting, 60 
Morphology, canid hybrids, 92 
Morton, J. R., 174 
Mother and stress, 183 
Mothering, effects, 163 

Murphree, O. D., 204, 227 
Muzzle-bite, 250 

Needs, human, 257 
Neophobia, 237 
Neoteny, 9, 151 

Nervous system, development, 

Nervous topologies, 222, 225 
Nervous typology, 205 
Nesbitt, W, H., 41, 67 
Newton, J. E. O., 228 
Noltebohm, F., 174 

Ontogeny. See development 
Orbrist, P. A., 228 
Organization of behavior, 238 
Origms of dog, 241 
Overattachment, 161 
"Overbreeding," 257 
Overindulgence, 161, 260 

Pack cohesion, 61 
Paedomorphic features, 8 
Parasites, 45 

Parasympathetic stimulation, 224 
Parental behavior, 11 
Pariah dogs, 244 
Pavlov, I. 181 

"Perpetual puppy" syndrome, 161 
Petting, and heart rate, 182; and 
stress, 183 
Phenodeviants, 238 
Phenotype, changes, 171; domes- 
tic fitness, 169; enhancement, 195 
Phylogeny of submission, 229 
Plasma cortisol, 202, 209 
Play, in canids, 133 
Predation, 27 
Prenatal influences, 165 
Prey-catching, 107 
Prey, dissection of, 116, 119 



Primary social attachments, 145 
Psychophysiological dependency, 

Psychosomatic disorders, 258, 
259, 260 

Reactivation, 238 
Relationships, man-dog, 257 
Reproduction and socioenviron- 
ment, 170 

Richter, C. P., 14, 18, 177, 223, 226 
Royer, F. L., 182 

Sackett, G. P., 158, 167 
Salzen, E. A., 158 
Schenkel, R., 80 

Schneirla, T. C., 83, 162, 205, 224, 


Scholander, P. F., 178 
Schutz, F., 157 

Scott, J. P., 37, 41, 143' ^56' ^59' 
171, 172, 174, 179/ 182, 188, 189, 
236, 243, 247, 248/ 250 
Scott, M, D., 51 
Screams, 76 

Secondary socialization, i43' 
Selective breeding, 15 
Sensitive periods, 171 
Sex, and environment, 170; and 
sociability, 147 
Sexual behavior, 11, 37 
Sexual maturity, 148, 253 
Shyness, 95, 97 
Silber, R. H., 269 
Silver, H., 91 

Sociability and territory, 246 
Social behavior, feral dogs, 5® 
Social bonds. See socialization 
Social deprivation, 159 
Social homeostasis, 232 
Social inhibition of aggression, 13° 
Social organization, 24, 26 

Social regression, 159 
Socialization, 14, 39, 141, 156/ 160; 
of dog and cat, 158; and heart 
rate, 212; and touch, 184 
Socioecology, 21 
Sociosexuai discriminations, 149 
Somatotypes, hybrids, 95 
Sounds, vocal, 72 
Speciation, artificial, 7 
Species-typical actions, 139 
Spermatogenesis, seasonal, 253 
Spitz, R., 162, 184, 224 
Staines, H., 21 
Stereotypes, 168 
Strangers, fear of, 142 
Stress, handling, 189 
Stress resistance, 164, 189 
Structure and domestication, 248 
Submission, evolution of, 229; 
and heart rate, 219 
Sudden death, 225 
Supracaudal gland, 95 
Sympathetic tone, 34 

il gland, 251 
il posture, 250 
ming, 3' 4' 

<onomy of canids, 23 
aibrock, G., 7^' 80, 5 ' 
„perament, and 3 " 

,d handling, 165; “nd hurt 

ite, 177, 209, 

jterogeneity. 32 
nperature and actrvny, 48 

nporal sequencing m prey Wl 

IK, 107, 120 

nporary packs, 84 - hs 

Titoriality, 246 

;bcrge, J- B ■ 7 - 

,ntas, A , 165. ' 97 , 

rmpson, W R , .hi 

■eshold of acuoni, .-h 

THE dog: rrs domestication and behavior 


Timidity, 95, 97; and heart rale, 

Tonic immobility, 183, 224, 229 
Tooth eruption, hybrids, 95 
Trophotropic tuning, 205 
Trumler, E., 237 

Urination, social, 52 

Vagal inhibition, 185 
Vandenberg, J. G., 170 
Van Lawick, H., 28, 35 
Vauk, G., 128 

Vocalizations, 25, 69; group, 29 
Vdlgyesi, F. A., 229 

Wallace, R. K., 232 
Weber, E., 177 
W-eliciting sounds, 84 
Whines, 74 

Wild canids, behavior, 21; taming 
of, 141 

Wildness, 95 
Winter, P., 86 
Wolf, S., 178 
Wolf ancestry, 248 
Wolf-dog comparisons, 253 
Woolpy, J. H., 14, 143, 159 

Yelps, 75 

2 euner, F. E., 5, 6 
Zimen, E., 151